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Chapter 3
Evolution and Diversity of Bark
and Ambrosia Beetles
Lawrence R. Kirkendall
1
, Peter H.W. Biedermann
2
, and Bjarte H. Jordal
3
1
Department of Biology, University of Bergen, Bergen, Norway
2
Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena,
Germany
3
University Museum of Bergen, University of Bergen, Bergen, Norway
1. INTRODUCTION
“No other family of beetles shows such interesting habits as
do the members of the family Ipidae.”
—Milton W. Blackman, 1928
Most wood-boring insect species only tunnel in wood as
larvae. Their adults are free-flying insects that must move
about the landscape to encounter mates, find food, and locate
oviposition sites; in so doing, they face a myriad of inverte-
brate and vertebrate predators, and must deal with the
vagaries of wind, temperature, and precipitation. A few
beetles, however, have evolved to spend nearly their entire
adult lives inside woody tissues. Bark beetles (Scolytinae)
and pinhole borers (Platypodinae)—which we will refer
to collectively as bark and ambrosia beetles—are weevils
that have lost their snouts and that spend most of their adult
existence ensconced in dead wood (occasionally, in other
plant tissues), and by many measures, they are the most
successful lineages to do so. In this chapter, we will doc-
ument and discuss the striking variability in biology of these
weevils.
Wood is important to humans in many ways, and bark
and ambrosia beetles are abundant in forests and planta-
tions, so it is not surprising that there is a long history of
interest in these relatively small and nondescript insects.
Carl Linnaeus, the father of modern taxonomy and one
of the founders of ecology, described five species of
Scolytinae, including four of the most common European
species, which he described in 1758 (Trypodendron domes-
ticum,Tomicus piniperda,Polygraphus poligraphus,Ips
typographus, and Pityogenes chalcographus)(Linnaeus,
1758). There are Scolytinae and Platypodinae in the beetle
collections of the fathers of evolutionary theory, Charles
Darwin and Alfred Russel Wallace, and the latter even pub-
lished on them (Wallace, 1860). It is only in the first half of
the 20th century though that we first began to be aware of
the wealth of details of their fascinating but cryptic lives.
1.1 Topics and Taxonomic Coverage
We will focus on the evolution and ecology of feeding and
breeding biology, especially mating systems and social
behavior. Much of this variation is little known outside of
a small circle of specialists, as the vast majority of basic
and applied research in Scolytinae and Platypodinae is
focused on a handful of serious forest and agricultural pests
that have considerable economic and ecological impact.
Though well deserving of research, these taxa are not rep-
resentative of bark and ambrosia beetle biology as a whole.
We will not cover population ecology or pheromone
biology, as these topics are much more widely known
and have been thoroughly addressed in many research
and review articles, in this book (Chapters 1,4, and 5), as
well as in other books, e.g., Chararas (1962),Berryman
(1982),Mitton and Sturgeon (1982),Speight and
Wainhouse (1989),Lieutier et al. (2004), and Paine
(2006). We will also let others review in detail the growing
and fascinating topic of relationships with fungi and other
symbionts (but see Section 3; Chapter 6).
There are currently 247 genera of recognized Scolytinae
(see Appendix), most of which breed predominantly or
entirely in angiosperms (Figure 3.1); 86% of these genera
are represented in the tropics or subtropics, and 59% are
restricted to these warmer regions (Chapter 2). In terms
of numbers of species, 79% (four of five) are found pri-
marily in tropical or subtropical ecosystems. Less than
1% of the ca. 6000 Scolytinae species regularly kill healthy
standing trees, and from the existing literature it seems
unlikely that more than 5 to 10% occasionally do so (but
see Section 3.9).
Books dealing with the biology of Scolytinae (or of Sco-
lytinae plus Platypodinae) often reflect biases towards
species breeding in temperate conifer forests or vectoring
pathogens with significant impact on urban or ornamental
broadleaf trees (e.g., Chararas, 1962; Mitton and
Sturgeon, 1982; Lieutier et al., 2004). It is hoped that this
Bark Beetles. http://dx.doi.org/10.1016/B978-0-12-417156-5.00003-4
©2015 Elsevier Inc. All rights reserved. 85
chapter can help to redress this imbalance (see also
Chapters 1,11, and 12).
For less (in)famous bark and ambrosia beetles, in-
formation on ecology and behavior can be gleaned
from regional or global faunal works by, for example,
Thomas Atkinson and colleagues (see references), Roger
Beaver (see references), Cyril Beeson (1941), Maulsby
Blackman (Blackman, 1922; Blackman and Stage, 1918,
1924), Francis George Browne (1961), Willard Joseph
Chamberlin (1939, 1958), Constantin Chararas (1962),
L. G. E. Kalshoven (1959, 1960b), Akira Nobuchi
(1972), Karl E. Schedl (1961, 1962a, b), James Malcolm
Swaine (1918), and Stephen L. Wood (1982, 2007). Besides
the sources of natural history information mentioned above,
there are recent, more quantitative treatments of bark and
ambrosia beetle ecology, biogeography, and phylogeo-
graphy: ecological aspects of bark and ambrosia beetle
biodiversity (Ødegaard, 2000, 2006; Ødegaard et al.,
2000, 2005; Hulcr et al., 2007, 2008a, b; Novotny et al.,
2007, 2010); island biogeography (Kirkendall, 1993;
Jordal et al., 2001); and phylogeography (Cognato et al.,
1999; Jordal et al., 2006; Maroja et al., 2007; Cai et al.,
2008; Schrey et al., 2011; Garrick et al., 2013; Jordal and
Kambestad, 2014).
*
*
*
*
*
*
*
*
*
*
*
Conifer host plant
Broadleaf host plant
FIGURE 3.1 Phylogenetic tree of Scolytinae indicating associations with broadleaf and conifer host plants. The tree used here and in Figures 3.4
and 3.7 summarizes phylogenetic results based on molecular data with unresolved relationships resolved in part based on morphological evidence
(Normark et al., 1999; Farrell et al., 2001; Jordal et al., 2008, 2011; Jordal and Cognato, 2012).
86 Bark Beetles
Only a few aspects of bark beetle evolutionary biology
have been reviewed for Scolytinae (or Scolytinae and Pla-
typodinae) as a group: mating systems (Kirkendall, 1983);
inbreeding and other sources of biased sex ratios
(Kirkendall, 1993); the evolution of social behavior
(Kirkendall et al., 1997); and the evolutionary history of
bark beetles and pinholes borers (Jordal et al., 2011;
Jordal, 2014a, b, c;Chapter 2).
1.2 Why We include Platypodinae
We have chosen to include Platypodinae (“pinhole borers”)
in our chapter (as Hulcr et al. did in Chapter 2), primarily
with respect to mating and social behavior. The extreme
morphological similarity of Platypodinae to Scolytinae
has bedeviled systematists for decades, and highlights the
importance of convergent evolution in wood-tunneling
beetles (Figure 3.2). Pinhole borers were long treated by
entomologists as a separate family, closely related to “Sco-
lytidae.” More recently, phylogenies based on molecular
and morphological characters strongly suggest that this
group, too, is a highly derived group of weevils, but the Pla-
typodinae may not even be closely related to Scolytinae
(reviewed in Chapter 2, but also see McKenna et al.
(2009),Jordal et al. (2011),McKenna (2011),Haran
et al. (2013), and Gillett et al. (2014)).
Virtually all broadly oriented bark beetle specialists
have worked with both groups (and usually primarily or
exclusively these two), which until recently were con-
sidered to be two very closely related but separate families,
Platypodidae (ca. 1400 species) and Scolytidae (ca. 6000
species). Platypodine biology seems to only be known to
Scolytinae researchers and a few generally oriented forest
entomologists: we are not aware of the existence of any spe-
cialists who restrict their focus to Platypodinae. It has
become common practice to include both Scolytinae and
Platypodinae in taxonomic, faunistic and ecological works,
and until fairly recently to refer to them jointly as “Scoly-
toidea” (Hubbard, 1897; Blackman, 1922; Beal and
Massey, 1945; Pfeffer, 1955, 1995; Schedl, 1962b, 1974;
Chamberlin, 1939, 1958; Kalshoven, 1960a, b; Browne,
1961; Nunberg, 1963; Nobuchi, 1969; Bright and Stark,
1973; Beaver and Browne, 1975; Kirkendall, 1983;
Atkinson and Equihua-Martı
´nez, 1985a; Wood and
Bright, 1987, 1992 and subsequent supplements; Beaver,
1989; Atkinson and Peck, 1994; Kirkendall et al., 1997).
Scolytine and platypodine ambrosia beetles are frequently
collected together in dead and dying trees. Platypodinae
are strikingly similar to monogynous scolytine ambrosia
beetles in gross morphology, tunnel system architecture,
use of chemical and acoustic signals, mating behavior,
social behavior, and relationships with symbiotic fungi.
All but the most basal platypodines are monogynous
ambrosia beetles with extensive parental care; one species,
Austroplatypus incompertus (Schedl), is notable for being
eusocial (Kirkendall et al., 1997).
2. WHAT ARE BARK AND AMBROSIA
BEETLES?
2.1 Phylogenetics
Why tunnel? Foraging in the green is a dangerous place.
Being exposed to parasitoids and predators—and occa-
sionally extreme competition from hyperdiverse insect
communities—as well as to wind, rain, and occasional
extreme temperatures can generate a selective advantage
for a complete life cycle inside dead plant tissues. Although
less nutritious, such resources are less hostile in terms of
physical and chemical defenses mustered by live plants.
In fact, life under bark has evolved multiple times in
weevils (McKenna et al., 2009; Jordal et al., 2011; Haran
et al., 2013; Gillett et al., 2014)(Figure 3.2). Most, or
AB
FIGURE 3.2 Convergence in wood-boring weevils: the genus Homoeometamelus (subfamily Baridinae or Conoderinae, tribe Menemachini).
(A) Lateral view; note the lateral socketed teeth on all tibiae (arrows), of the same type as in many Scolytinae. (B) Mating niche with longitudinal
egg tunnel; arrows point to eggs laid in niches.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 387
perhaps all, wood-boring groups are old, originating at least
some 90–120 millions of years ago (Ma). The oldest sco-
lytine fossil is known from Lebanese amber that dates back
to Mid-Cretaceous some 120 Ma (Kirejtshuk et al., 2009).
This is about the same age as the oldest known Curculio-
nidae known from the Santana formation in Brazil
(116 Ma) (Santos et al., 2011). The Lebanese amber fossil
Cylindrobrotus pectinatus Kirejtshuk, Azar, Beaver, Man-
delshtam and Nel is not closely related to any extant or
fossil lineage of Scolytinae, but has all defining morpho-
logical characters of a bark beetle. Another fossil
(100 Ma) from Burmese amber belongs to the current genus
Microborus, which may indicate that Scolytinae was well
established as a dominant group already at that time
(Cognato and Grimaldi, 2009).
Platypodinae has a less documented fossil record, but is
represented by tesserocerine and platypodine inclusions in
Mexican, Dominican, Sicilian, and Rovno ambers (Schedl,
1972; Bright and Poinar, 1994). This group is much older,
however, and two fossils from Burmese amber indicate pos-
sible tesserocerine affinity (Cognato and Grimaldi, pers.
commun.), in accordance with molecular age estimates
(McKenna et al., 2009; Jordal et al., 2011).
The exact phylogenetic position of Scolytinae is
uncertain, but it is now well documented that this group
originated at the same time as modern phytophagous curcu-
lionids (McKenna et al., 2009; Jordal et al., 2011; Haran
et al., 2013; Gillett et al.,2014). Soon after the split between
the broad-nosed weevils and most other groups of advanced
weevils, Scolytinae makes up a consistently monophyletic
group closely related to typical long-nosed weevils such
as Molytinae, Cryptorrhynchinae, Baridinae, Curculio-
ninae, and Cossoninae. They may not be closely related to
Platypodinae, which seem more closely related to
Dryophthorinae than to Scolytinae (McKenna et al., 2009;
Gillett et al., 2014).
It seems certain that the wood-boring habit evolved
from external feeding on green leaves. Herbivorous Scoly-
tinae exist today, but none of these are basal lineages in the
phylogenetic tree of bark and ambrosia beetles. The closest
match is the Scolytini genus Camptocerus, where adults
feed on green leaves before tunneling into the bark to breed
(Smith and Cognato, 2011). With rare exceptions, Scoly-
tinae are restricted to denser, drier plant tissues such as
those in stems and branches of trees and shrubs. Few taxa
can deal with the typically soft, very moist tissues asso-
ciated with herbaceous plants. Even most species catego-
rized as “herbiphagous” breed in the dense supportive
tissues of stems or leaf petioles, not in leaves.
2.2 General Morphology
Bark and ambrosia beetles are highly adapted morphologi-
cally and ecologically to this unusual lifestyle and to the
special challenges of constructing and living nearly their
entire adult lives in tunnels. The adaptation to a life in con-
cealed niches in dead lignified plant material apparently
followed a distinct selection regime with consequences
for morphological change. The change in diet from green
leaves to bark, wood or fungi has modified both the external
chewing appendages as well as the internal digestive
system. Boring in bark and wood also dramatically changed
their reproductive biology due to control of valuable
resources in the form of durable, protective tunnels. Control
of access to the tunnel by the opposite sex has therefore led
to a variety of behavioral and morphological changes in the
context of optimal mate choice. Maintenance and pro-
tection of tunnels has furthermore led to changes in mor-
phology to optimize movement in the tunnel, shoveling
of frass, and the blocking of the entrance hole.
Life in tunnels and caves places obvious restrictions on
body shapes, since protuberant body parts would limit
movement and flexibility. Adult beetles that bore into wood
are generally cylindrical, as are bark and ambrosia beetles
(Haack and Slansky, 1987). In addition, all bark and
ambrosia beetles have large, flattened eyes and short
antennae that can be folded into the body. A unique feature
involves vertically enlarged eyes, which extend from the
vertex to the gula, sometimes slightly or even completely
divided where the antennal scape attaches and folds back.
It is not known if eye enlargement has evolved due to a life
in near darkness, but we note that certain weevil groups,
which do not tunnel as adults (such as many conoderines),
also have large, flat, contiguous eyes.
Excavation of tunnels requires a considerable biting
force, and scolytines and platypodines have larger man-
dibles than most other weevils. Mandibles are short and
thick, and have strong muscles attached (Schedl, 1931).
The chewing procedure varies depending on whether the
woody tissue is ingested for food or simply chopped up
to be removed, as in most ambrosia beetles. These bore
new tunnels by cutting with their mandibles during back
and forth movements of the head and rotation of the whole
body within the tunnel. By contrast, when feeding, they
crop the enlarged nutritious spores (“ambrosial growth”)
of their fungi by horizontal movements of the maxillae
(which have comb-like hairs or structures at the end) and
swallowing movements of the labrum. Effective chewing
of wood bits is enabled by a flexible rotating head with
strong muscle attachments.
Wood-boring beetles are generally well equipped with
cuticular structures that aid in pushing and scraping, such
as various spines and socketed denticles on the tibiae (pen-
ultimate leg segment) (Swaine, 1918). While a terminal
tibial spine (uncus) is commonly seen across the weevils,
many scolytines have additional socketed denticles along
the lateral edge of the tibiae. These denticles are typically
evolved from ordinary hair-like setae, and their socketed
88 Bark Beetles
origin is clearly visible (Wood, 1978), although they are
sometimes reinforced and overgrown by cuticle (Jordal,
1998). It is unclear how important such denticles are for
wood-boring beetles given that several groups are lacking
denticles, such as Scolytus and close relatives, most
wood-boring cossonines, and in Platypodinae, the latter
instead have developed sharp ridges and rugae on their pro-
tibiae (Strohmeyer, 1918). On the other hand, we do see
similarly developed denticles in unrelated wood-boring
groups such as Amorphoceriini (Molytinae), Araucariini
(Cossoninae), Campyloscelini (Baridinae), and in certain
bostrichid wood borers as well as for digging insects in
general (e.g., scarabs) (Figure 3.2).
Some scolytines are cleptoinquilines, and take over
ready-made nests of ambrosia beetles, killing or ejecting
the original tenants in the process. These species have
developed dramatic features such as a sharply prolonged
anterior pronotum and various elaborately sculpted sharp
elongations of the declivity; the former often takes the form
of a pointed hood with or without a terminal hook
(Figure 3.3F). Nest parasitism is most common among
corthylines in the genera Tricolus and Amphicranus and
AB
E
D
C
GF
FIGURE 3.3 Morphology of Scolytinae. (A, B) Sexual dimorphism, here represented by different shapes of the frons. (A) Male and female Scolyto-
platypus rugosus Jordal. (B) Male and female Phrixosoma concavifrons Jordal. (C–E) Extreme sexual dimorphism in an inbreeding bark beetle. (C) Male
(left) and female (right) siblings of Ozopemon uniseriatus Eggers. (D) Head features of the male. (E) The male is fully developed and reproductively
mature, note the aedeagus. (F, G) Examples of declivity variation. (F) Amphicranus fastigiatus Blandford, holotype. (G) Tomicus piniperda (L.).
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 389
in the xyleborine genus Sampsonius. As with declivital
teeth and spines in Scolytinae and Platypodinae
(Hubbard, 1897; Hamilton, 1979), it is likely that acute
developments on the front and back end of the cleptoinqui-
lines are used in fighting and tunnel defense. Other weevil
groups also take over ambrosia beetle tunnels, for instance
in Brentidae (Kleine, 1931; Beeson, 1941; Roberts, 1969;
Sforzi and Bartolozzi, 2004) and in the baridine subtribe
Campyloscelina (Schedl, 1972; Thompson, 1996), and
these show strikingly similar morphological adaptations.
Life in tunnels has led to multiple origins of fungus
farming, including 10 times or more in Scolytinae and once
in Platypodinae (Jordal and Cognato, 2012). Shifting from
consuming woody to fungal tissues (which are softer and
require less chewing) selects for changes in mouthpart
and digestive tract morphologies. While phloem-feeding
bark beetles have their maxillary laciniae fringed by coarse
bristle-like setae, those feeding solely on fungal mycelium
and conidia have very fine hair-like setae (Jordal, 2001).
We see the same trend in the proventriculus that is situated
in the alimentary tract in the prothorax and which functions
like the gizzard of birds (Nobuchi, 1969). The normal con-
dition for a bark beetle is to have a strongly sclerotized pro-
ventriculus with a large anterior plate containing nodules,
teeth or transverse ridges. All ambrosia beetles have their
anterior plate strongly reduced or totally absent. Remnants
of the anterior plate are most evident in some of the most
recently evolved lineages of ambrosia beetles such as Xyle-
borini and Premnobiina (Ipini), each roughly 20 million
years old (Jordal and Cognato, 2012; Cognato, 2013). In
each of these groups, the anterior plate is clearly visible,
but very short and less sclerotized.
Finally, access to a tunnel for food and reproduction is
limited in the sense that the tunnel-initiating individual can
control access. This has consequences for mate recognition
and mate choice, and for how late arrivals such as nest par-
asites and predators are rejected. The largest variation in
morphological traits is therefore not surprisingly seen in
body parts associated with tunnel blocking (discussed
further in Section 2.3). Morphological adaptations to
blocking the entrance to gallery systems are primarily seen
in the declivity. Many taxa have evolved various teeth,
knobs, and ridges on the declivity. Though there are few
observations and no experiments on the function of these,
Hubbard (1897) and Hamilton (1979) have hypothesized
that especially the sharp teeth often seen on the borders
or apex of the declivity function as weapons of defense
against potential rivals and natural enemies. The overall
shape of the declivity is likely also an adaptation to burrow
blocking, particularly in species with flat or convex decliv-
ities, as the back end of the beetle ideally should fit the cur-
vature of the outer bark surface as seamlessly as possible.
This hypothesis could be tested by comparing the degree
of curvature of the declivity (for the blocking sex) with
the surface curvature of preferred host material, where
one would expect to find flatter declivities in species regu-
larly breeding in large diameter trunks and more strongly
curved declivities in species with strong preferences for
twig and small branches or thin stems.
Alternatively, in some taxa, the ventral aspect of the
abdomen may be partly or entirely involved in forming
the hind end of the beetle. In such cases, the apex rises more
or less sharply, involving all or just the last few sternites
depending on the group. The venter is only weakly raised
in Xyloctonus and certain cryphalines, but rises steeply from
the second ventrite in Scolytus and close relatives. In the
latter group, the venter completely takes over the role of
the declivity, in forming the hind end, which blocks the
entrance. Development of the venter in this manner is
extreme in the Platypodinae genera Doliopygus and Meso-
platypus (Strohmeyer, 1918; Schedl, 1972).
A cryptic lifestyle makes coloration less important for
wood-boring beetles compared to those living in the outside
world. Very few groups show any coloration beyond shades
of brown; the color of mature adults ranges from dark yellow
to reddish brown to black. The only significant exception to
this pattern is found in three species of Camptocerus, a genus
closely related to Scolytus (Smith and Cognato, 2010, 2011).
The metallic green to bronze shine is unique to these species
(see Fig. 2.7 in Chapter 2). Although the function of the
metallic shine is completely unknown, it is interesting that
species in this genus are also unique in spending extended
periods aggregating and feeding on green leaves, before
moving into wood (Smith and Cognato, 2010, 2011).
Scolytinae beetle bodies are usually 2–3 times as long as
wide and fairly parallel sided; they vary in size from ca.
0.5 mm to a little over a centimeter in length, and most
species fall in the range 1 to 4 mm long. There is no strong
correlation between diameter of breeding material and body
size: one finds small species that prefer larger trunks, and
medium to large species that breed in branches or even
twigs. Platypodines are more slender and on average longer,
and they are more frequently confined to trunks and
medium to large branches than are scolytines. Browne
(1961) has speculated that there may be an evolutionary
trend towards small body size, driven by selection for
escaping predators that use tunnel entrances to get into
gallery systems, especially with respect to ambrosia beetles.
This intriguing hypothesis has yet to be tested compara-
tively. Scolytinae as a group are the smallest of the major
groups of wood-boring insects, and platypodines are among
the smallest (Haack and Slansky, 1987).
Within species-specific limits, body size of wood-
boring beetles such as scolytines and platypodines is
generally determined by the quality and amount of food
consumed by larvae (Andersen and Nilssen, 1983;
Kirkendall, 1983; Haack and Slansky, 1987; Kajimura
and Hijii, 1994). Resource quality, in turn, is affected
90 Bark Beetles
strongly by factors such as how fresh or old the breeding
material is, remnants of defensive chemicals, and presence
of fungi and microorganisms, while quantity is affected by
factors such as inner bark thickness (for phloeophagous
species), tunnel length (for ambrosia beetles), and density
of competing larvae of the same or different species. Body
size is important in natural selection (fecundity, survi-
vorship), and sexual selection (fighting, mate choice), and
affects features such as survival in cold temperatures
(e.g., Dendroctonus;Safranyik, 1976), attractant pher-
omone production (Anderbrandt et al., 1985), and anti-
aggregation pheromone production (Pureswaran and
Borden, 2003).
2.3 Sexual Dimorphism
Sexual selection is a powerful evolutionary force (Darwin,
1859; Shuster and Wade, 2003), and has surely been a prime
factor in the evolution of sex differences in bark and
ambrosia beetles. Dimorphic features are especially
common in the frons (Figure 3.3) and declivity, and often
in the underside of the abdomen (venter). This is to be
expected, since characters involved in mating behavior
(primary and secondary sexual characters) often evolve
more rapidly than other morphological features (Civetta
and Singh, 1999), and the frons, declivity, and venter are
directly involved in mating behavior. As is often the case,
the features exhibiting sexual dimorphism are frequently
the best characters for separating closely related species,
and are presumably used by the beetles themselves in
species recognition as well as mate recognition.
Courtship in both Scolytinae and Platypodinae involves
primarily tactile, chemical, and acoustic stimuli. Typically,
the courting sex rubs or bumps the frons against the
declivity or venter of the first arriving sex. There is evi-
dence for specific types of setae in these body regions that
match between the different sexes of a species, such as in
Scolytus (Page and Willis, 1983). Species in many out-
breeding bark and ambrosia beetle genera are therefore
diagnosable mainly based on extravagant sculpturing or
ornamentation (such as long setae) seen in only one of
the sexes, commonly of the frons (Figure 3.3). Very gen-
erally, the frons of the courting sex is frequently flat or
concave, while that of the colonizing sex is convex, and
frequently the frons of the courting sex has longer or
denser setae (S. L. Wood, 1982). In species with a
dimorphic frons, individuals of the courted sex from
closely related species might be identical in frons features,
while frons characters are diagnostic in the courting sex. If
there is noticeable sexual dimorphism in features of the
declivity, such as degree of concavity or presence and size
of teeth or spines, these characters are most developed in
the courted (pioneering) sex. However, both frons and
declivity can be monomorphic or nearly so; it is not clear
why some species are distinctly sexually dimorphic and
others not so.
Characters other than the frons and declivity can be sex-
ually dimorphic as well. Some of these, such as modifica-
tions of the antennae, or of the shape or setation of the
last ventral abdominal segment, are certainly associated
with acquiring mates or with copulation, but others (such
as modifications of legs or pronota) may be adaptations
to differences in sex roles (including differences in which
sex carries symbiotic fungi). The basal antennal segments
may differ in shape and setae pattern. For example, indi-
viduals of the courting sex (females) in most Micracidini
have dense, long setae on the antennal scape, which are
not present in the pioneering sex (males); a similar antennal
scape dimorphism occurs in Chramesus and some Campto-
cerus, but in these genera it is males who court and who bear
the long setae on the scape (S. L. Wood, 1982). In Campto-
cerus noel Smith and Cognato, it has been confirmed that
the setal brush on the scape is used quite actively in
courtship (Smith and Cognato, 2011). In many corthyline
ambrosia beetles, the antennal club is enlarged (extremely
so in Corthylus) and may be different in shape in females
(the courting sex). The pronotum is differently shaped in
Trypodendron (S. L. Wood, 1982), and in some groups
(such as Phloeoborus,Scolytoplatypus, some Cryphalus,
and some Scolytodes) the sexes differ in surface sculpture
of the pronotum. The sexes of Scolytoplatypus differ dra-
matically in the protibiae and procoxae (segments of the
first pair of legs). The protibiae of females have a rougher
surface and more strongly developed teeth (Beaver and
Gebhardt, 2006; Jordal, 2013), characters that we speculate
might be an adaptation to fungus farming in these ambrosia
beetles.
An additional difference between the sexes (occa-
sionally the only one) is body size. Although the pattern
has yet to be investigated systematically, it is clear from
the average measurements in taxonomic treatments (such
as S. L. Wood, 1982, 2007; Jordal, 1998) that, where size
differences exist, it is the pioneering sex that is the larger.
This is generally associated with mating system, females
being the larger sex in monogynous species and males in
harem polygynous species (see also Foelker and
Hofstetter, 2014). This pattern for size dimorphism in out-
breeding species may arise from differences in selection on
the two sexes. Females are generally larger in insects,
including weevils, probably because of fecundity selection
on females being stronger than any selection for large size
in males. However, in harem polygynous species, there is
likely both intrasexual and intersexual selection for large
male size (males being the pioneering sex, and the sex with
greater variance in reproductive success), and in these cases
this seems to be stronger than fecundity selection on con-
specific females.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 391
Sexual selection is presumably weak or absent in
extreme inbreeders, where many species frequently or reg-
ularly have only one male per brood. Interspecific differ-
ences in the frons of females from related species are
weak or nonexistent. Declivital differences do exist for
females of related inbreeding species, especially in xyle-
borines, but overall interspecific differences in groups of
related inbreeders seem to be much less than those found
in groups of related outbreeders.
Sexual dimorphism in extreme inbreeders takes a very
different form than that for outbreeding species, and is con-
sistent with patterns found in other regularly inbreeding
arthropods (Hamilton, 1967). Males of regularly inbreeding
Scolytinae are rare, and are usually smaller (considerably
smaller in many species), are less sclerotized, and are dif-
ferently shaped; they have reduced eyes (Vega et al.,
2014) and males cannot fly because the second pair of
wings is vestigial. Curiously, there are some striking excep-
tions. In certain unusually large species of Xyleborini (such
as the Xyleborus princeps group of species), males are very
similar to females in both size and shape. Cyclorhipidion
males are about the same size as females, but have the pro-
notum more elongated. Dendroctonus micans (Kugelann)
and its sister species D. punctuatus LeConte are unique
among inbreeding Scolytinae in their lack of significant
sexual dimorphism; in these species, males are very similar
to females in size, and can in fact fly (see Section 4.2). At
the other extreme is Ozopemon, a genus of haplodiploid,
phloeophagous inbreeding scolytines that comprise one of
only two examples in Coleoptera of larviform males
(Jordal et al.,2002). Sexual dimorphism is so extreme in
Ozopemon (Figure 3.3C–E) that for about 50 years the
rarely collected larva-like males were thought by some
leading beetle experts to belong to the family Histeridae
(Crowson, 1974).
One rare form of dimorphism in Scolytinae involves the
development of horn-like structures on the anterior (rather
than posterior) part of the body. Long horns are a particu-
larly striking feature of many Cactopinus species, where
they originate from the lower part of the frons. Various
forms of nodules or carinae are found on the frons of a
variety of scolytines, but the large size of these horns is a
unique feature for this genus. A few other genera have small
spines originating from the mandibles of the courting sex,
such as in male Triotemnus (Knı
´z
ˇek, 2010) and other dryo-
coetines, female Styphlosoma (S. L. Wood, 1982), female
Araptus araguensis Wood, Phelloterus females (Wood,
2007), or female Diapus in Platypodinae. At least for
Diapus, the mandibular teeth are dehiscent and only used
during courtship to pull out the pioneering male (Beaver,
2000). Mandibles are greatly enlarged in the courting sex
in Gnatholeptus females and Phelloterus females (Wood,
2007). The role in courtship behavior of these mandibular
adaptations is not known.
Dimorphism is also frequently expressed on the
declivity of the elytra. The blocking sex can have more
strongly developed or a larger number of spines, teeth, or
setae, and can have the declivity more flattened or concave
than in the other sex. Such differences are so pronounced in,
for example, the ambrosia beetle genera Amphicranus and
Gnathotrupes that specialists have occasionally initially
assigned males and females to different species or even dif-
ferent genera. However, it should be emphasized that sexual
dimorphism of the declivity in many genera is very mild or
nonexistent; in our experience, interspecific differences in
the declivity are more frequent than intersexual differences,
and are a great aid in separating closely related species.
Hypothesized functions of features of bark and ambrosia
beetle declivities have never been seriously analyzed or
studied experimentally, which is unfortunate given the
extraordinary variation that can be found within both Sco-
lytinae and Platypodinae.
The various shapes of spines and tubercles on declivities
may well serve several purposes, the most obvious possibil-
ities being mate recognition and effective shoveling
of frass. Though we can find few mentions of the idea in
the literature (as mentioned above, Hubbard, 1897 and
Hamilton, 1979), specialists often speculate in conversa-
tions that the sharp projections and borders seen in many
platypodines and scolytines may be stabbing or cutting
weapons useful against conspecific usurpers and natural
enemies trying to gain entrance to the gallery system.
Hubbard describes finding fragments of “vanquished”
males in the tunnel systems of Euplatypus compositus
(Say), an abundant North American platypodine ambrosia
beetle. He writes (p. 14):
The female is frequently accompanied by several males, and
as they are savage fighters, fierce sexual contests take place,
as a result of which the galleries are often strewn with the
fragments of the vanquished. The projecting spines at the
end of the wing-cases are very effective weapons in these
fights. With their aid a beetle attacked in the rear can make
a good defense and frequently by a lucky stroke is able to dis-
locate the outstretched neck of his enemy.
We mentioned earlier that there are taxa in which the
venter takes over part or all of the role of forming the hind
end of burrow-blocking bark and ambrosia beetles. Sexual
dimorphism in the venter of Scolytus, and many platypodine
genera, takes the form of differences in spines and setae,
exactly as with sexual dimorphism of declivities.
3. EVOLUTIONARY ECOLOGY
OF FEEDING
Scolytinae and Platypodinae are components of what are in-
creasingly being termed “saproxylic” beetle communities—
species associated with dead wood and associated structures
92 Bark Beetles
(such as woody fungi) (Ausmus, 1977; Swift, 1977;
Ahnlund, 1996; Hammond et al., 2001; Ulyshen et al.,
2004; Ødegaard, 2004; Tykarski, 2006; Lachat et al.,
2006, 2012; Zanzot et al.,2010). Host trees are usually
dead or severely weakened, and their colonization by
these beetles, which often carry with them a complex
community of fungi, bacteria, yeasts, and mites, initiates
the breakdown of plant tissues and recycling of nutrients.
Actually, bark and ambrosia beetles breed in a wide
variety of plant tissues. The feeding behavior of Scolytinae
and Platypodinae has traditionally been broken down into
categories based, first, on whether the larvae feed directly
on plant tissues or on cultivated fungus, and second, for
the direct plant feeders, on the tissues consumed by de-
veloping larvae. Since adults feed within their breeding
material, the substances consumed by larvae are normally
adult food as well (larvae in some ambrosia beetles feed on
fungus-infested wood, whereas adults only feed on fungal
tissues, but they here are both regarded as feeding
on farmed fungi; see Section 5.3). We adopt the categories
that have been standard for over five decades (Table 3.1).
However, as Beaver (1986) emphasizes, “[the beetles] do
not cooperate very readily in tidy classifications” (quoting
Browne, 1961). Though most species can easily be placed
in one of these categories, some feeding habits are hard to
classify, and our classifications in some cases could be dis-
puted. In this section, we will briefly describe the larval
feeding modes of bark and ambrosia beetles, with a focus
on more unusual habits, which are less well known than
phloem feeding or fungus tending.
As pointed out by many authors, many or most Scoly-
tinae (and all Platypodinae) are associated in one way or
TABLE 3.1 Traditional Classification of Larval Feeding Modes of Scolytinae and Platypodinae (Schedl, 1958; S. L. Wood,
1982, 1986, 2007). The Examples Given are not Exhaustive; for more Details, see Appendix
Larval Feeding
Mode Examples (see Appendix for complete list) Feeding
Herbiphagy Hylastinus obscures (Marsham) (where invasive), clover
roots; Thamnurgus euphorbiae (Kuster), stems of
Euphorbia;Xylocleptes bispinus (Duftschmid) in
Clematis;Coccotrypes rhizophorae Eggers, mangrove
propagules; petiole-breeding Scolytodes species.
Feeding on fresh or dry fleshy plant tissues, including
stems of herbaceous plants, leaf petioles, cactus
“leaves,” grass stems, mangrove viviparous
propagules.
Spermatophagy Most Coccotrypes;Conophthorus, developing
gymnosperm cones; Araptus, clade in legume seeds;
Pagiocerus frontalis (F.), Lauraceae and Zea seeds;
Hypothenemus obscures (F.), macadamia seeds,
etc.; Hypothenemus hampei (Ferrari), developing
Coffea fruits; Dactylotrypes, palm seeds.
Feeding in large hard seeds and the encompassing
fruit tissues.
Mycophagy Trischidias and Lymantor decipiens (LeConte),
ascomycete fruiting bodies in dry twigs or bark.
Feeding in free-living (not cultivated) fungi (but see
Harrington, 2005).
Myelophagy Pityophthorus (some); Araptus (some); Bothrosternini
(non-xylomycetophagous species); Cryptocarenus;
Micracisella;Hypothenemus (a few); Chramesus
(a few); Scolytodes (a few); Dendrocranulus, curcubit
vines.
Feeding in pith of twigs, small branches or small
stems, including small vines (e.g., Dendrocranulus in
cucurbit vines).
Phloeophagy Most Scolytinae, no Platypodinae: Dendroctonus,Ips,
Tomicus, most Scolytus, most Pityophthorus, etc.
Feeding in phloem tissues (inner bark), though some
larvae engrave outer sapwood; may or may not be
regularly associated with fungi which increase
nutritional value of the substrate.
Xylomycetophagy
(ambrosia beetles)
Platypodinae; Xyleborini; Scolytoplatypodinae;
Xyloterini; Hyorrhynchini; Corthylini-Corthylina;
Camptocerus;Hypothenemus (a few); Premnobius;
Scolytodes unipunctatus (Blandford).
Feeding on “farmed” ectosymbiotic fungi growing in
wood; larvae of some species also ingest wood.
Schedl’s (1958) original definition:
“larvae...feeding...upon the mycelia of fungi
cultivated on the walls of their tunnels.”
Xylophagy Dactylipalpus;Hylocurus,Micracis,Thysanoes;
Chramesus xylophagus Wood; Dendrosinus;
Phloeoborus; some Lymantor;Scolytodes multistriatus
(Marsham).
Feeding in xylem tissues (sapwood, never heartwood)
but not cultivating symbiotic fungus.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 393
another with fungi and other microorganisms (Six, 2013).
Phloeophagous bark beetle-vectored fungi have long been
known to be important in overcoming host defenses of live
trees, but their role in nutrition is only now being puzzled
out for a few model species. As more is learned about the
roles microorganisms play, we will be able to make finer
distinctions in feeding categories: one could separate out
species of Ips and Dendroctonus that feed in phloem
enriched with symbiotic beetle-borne fungi as “phloeomy-
cophagous,” for example (Six, 2012), and distinguish
between ambrosia beetles whose larvae feed purely on
fungus and those that also consume wood (Roeper, 1995;
Hulcr et al., 2007;Chapter 2). These distinctions make
sense biologically and reflect different morphological,
physiological, and behavioral adaptations, but the use-
fulness of such fine distinctions will remain limited until
we have investigated a broad selection of species. Oversim-
plified as it is, our categorization of larval feeding habits
does have considerable heuristic value and has been
essential in documenting and explaining major ecological
and evolutionary trends in these two subfamilies (Beaver,
1979a; Kirkendall, 1983, 1993; Atkinson and Equihua-
Martı
´nez, 1986a).
Larval feeding habits have consequences for patterns of
host usage. Generally, species breeding in live trees tend to
be relatively host specific, sometimes very narrowly so
(Section 3.9). Phloeophagous and herbiphagous species
are more host specific than species breeding in wood, pith,
seeds, or as ambrosia beetles (Beaver, 1979a; Atkinson and
Equihua-Martı
´nez, 1986b; Hulcr et al., 2007).
Larval feeding habits also have consequences for
fecundity, and thus for suites of interrelated life history
traits. Plant tissues are generally a poor resource from the
point of view of nutritional quality, being much lower in
nitrogen than beetle bodies (White, 1993; Ayres et al.,
2000). Fresh and particularly living phloem is a better
resource than older, dead inner bark (Kirkendall, 1983;
Reid and Robb, 1999). Inner bark and seeds are much higher
in nitrogen than wood or pith. However, ambrosia fungi and
some fungi associated with phloem feeders (Section 3.1) are
rich in nitrogen (French and Roeper, 1975; Ayres et al.,
2000); ambrosia fungi concentrate nitrogen, and have much
higher amounts than the wood itself (French and Roeper,
1975). That pith, wood, and woody leafstalks are unusually
poor in nutrition is reflected in the fact that scolytines
breeding in these substrates have considerably lower
fecundity than those breeding in inner bark or seeds
(Kirkendall, 1983, 1984; Jordal and Kirkendall, 1998).
For detailed insight into the ecology of bark and
ambrosia beetle feeding see general resources such as the
works in our reference list by Beeson, Blackman, Browne,
Kalshoven, Schedl, or Wood, review papers by Kirkendall
(1983, 1993; Kirkendall et al., 1997) and Beaver (1977,
1979a, b) and the research papers by, for example, Atkinson
and collaborators (Mexico, S. E. US), Blackman (eastern
US), Beaver (worldwide), Cognato and collaborators
(Hulcr, Smith, and others) (worldwide), and, for fungus
farming in particular, by Hulcr, Cognato, Jordal and collab-
orators Six, and Harrington.
3.1 Phloeophagy (Breeding in Inner Bark)
Of woody tissues, inner bark is the richest, especially in
nitrogen (Cowling and Merrill, 1966; Kirkendall, 1983),
so it is no surprise that the most primitive Scolytinae breed
in dead inner bark of trunks and branches (Figures 3.4 and
3.5), or that phloem feeding is the most widespread larval
feeding mode. Roughly half of all Scolytinae genera are
wholly or partly phloeophagous, and 20 of 26 tribes have
at least some phloeophagous species in them (Table 3.2;
Figure 3.4). Only phloeophagous species are known from
Hylastini, Phloeotribini, and Polygraphini, and several
other tribes are primarily phloeophagous (Appendix).
3.1.1 Phloeophagous with Some
Consumption of Wood
In certain phloeophagous species in hardwoods, older
larvae (often the final instar) tunnel in the outermost
sapwood, and pupate in the wood. Thus, late-stage larvae
of Scolytus muticus Say, which breeds in Celtis (hackberry),
burrow “for some distance” in the sapwood, “...and if they
are at all numerous soon reduce the outer part of the wood
and bark to a mere shell” (Blackman, 1922). Triotemnus
pseudolepineyi Knı
´z
ˇek larvae consume all phloem and
sapwood, when breeding in branches of the shrub
Bupleurum spinosum Gouan (Apiaceae) in Morocco
(Knı
´z
ˇek, 2010). Other examples include Chramesus
hicoriae LeConte (Blackman and Stage, 1924); Phloeo-
sinus sequoia (Hopkins) (De Leon, 1952); Strombophorus
ericius (Schaufuss) (Browne, 1963); and species of Hylur-
gonotus and Xylechinosomus breeding in Araucaria (Ru
¨hm,
1981; Jordal and Kirkendall, pers. observ.).
Sapwood is roughly an order of magnitude lower in
nitrogen than inner bark and more heavily lignified
(Cowling and Merill, 1966; Haack and Slansky, 1987);
therefore, phloeophagous larvae should avoid feeding on
it, if possible. It is possible that fungi nutritionally improve
the wood quality for beetles, but this has not been studied.
One possible hypothesis for “late-stage xylophagy” is that
in thin-barked hosts, larvae simply are forced to consume
wood as they get larger (Browne, 1963); in many species,
bark beetle larvae are small enough to be able to feed
entirely in inner bark, but in others, the amount of wood
consumed will be inversely proportional to the diameter
of the breeding material. A second hypothesis is that bur-
rowing into the wood makes it more difficult for parasitoid
94 Bark Beetles
wasps to locate and parasitize larvae. Additionally, wood
might be less strongly infested by potentially harmful
microbial pathogens than more nutrient-rich phloem. Many
bark beetles pupate in the sapwood, in some cases tunneling
directly inwards to do so; this likely is an adaptation to
reducing parasitism. Testing the second hypothesis is
self-evident; a test for the first hypothesis would be to
compare resultant body size of offspring that do not feed
on sapwood as larvae (larval tunnels do not engrave the
wood) with those that do consume much sapwood as larvae
(their tunnels clearly etching the wood).
3.1.2 Feeding on Phloem Nutritionally
Improved by Fungi
Insects breeding in dead woody tissues will always have
constant interactions with a variety of mites, nematodes,
fungi, and bacteria (Hamilton, 1978). Bark and ambrosia
beetles are an optimal vehicle for transport of mites,
nematodes, fungi, and bacteria from old host material to
new, and many hitch rides on them (Stone, 1990; Paine
et al., 1997; Six, 2003, 2012; Harrington, 2005; Cardoza
et al., 2006a; Hofstetter et al., 2006; Knee et al., 2013;
*
*
*
**
*
*
*
*
*
*
*
*
*
Ambrosia fungus
Sapwood
Herbs
Seeds
Phloem
*
*
FIGURE 3.4 Phylogenetic tree of Scolytinae with feeding modes indicated (see inset legend). Stars indicate genera or lineages (if on a node) in which
the feeding mode is rare (one or just a few species).
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 395
Shimizu et al., 2013; Susoy and Herrmann, 2014;
Chapter 6). Some small organisms perform useful functions
from the beetle’s point of view, and many bark and
ambrosia beetles have morphological adaptations that
increase the likelihood of successful transport of helpful
symbionts. In particular, a wide variety of species have
developed external crevices, pits, simple pockets, or
complex invaginations somewhere on the body, for tra-
nsporting fungi (and perhaps other microorganisms)
(Beaver, 1988; Harrington, 2005; Six, 2012); these struc-
tures are often bordered by setae, which help in combing
fungal spores into the receptacle. Most species with such
structures are ambrosia beetles (discussed below and in
Section 5.1), but some breed in inner bark and feed on
phloem they have inoculated with fungi they have intro-
duced. There are also phloeophagous species with con-
sistent associations with fungi but which have no special
structures for transporting them, including D. pseudotsugae
Hopkins, D. rufipennis Kirby, Ips avulsus (Eichhoff), and
Tomicus minor (Hartig) (Beaver, 1988).
Many species even have structures for transporting fungi
from host to host in more or less sophisticated cuticular
invaginations or pits known as mycetangia (Francke-
Grosmann, 1956a) or mycangia (Batra, 1963). Larvae of
phloeophagous species that are associated with fungi
feed (at least in most stages) in woody tissues, not on mats
of fungal hyphae. The earliest research into mycetangia
revealed their presence in phloeophagous as well as
xylomycetophagous species (Francke-Grosmann, 1956a,
b, 1963a, b, 1965, 1966; see Kirisits, 2004). Francke-
Grosmann (cited above) reported mycetangia in typical
phloeophagous species in Hylastes,Hylurgops, and Ips.
The potential nutritional benefits of fungi in species that
are not ambrosia beetles are now being explored in detail
(Six and Paine, 1998; Ayres et al., 2000; Bentz and Six,
2006; Adams and Six, 2007; recent reviews by Six, 2012,
2013;Chapters 6 and 8).
Several phloeophagous Ips species have mycangia,
including the Eurasian Ips acuminatus (Gyllenhal)
(Francke-Grosmann, 1963a). This Ips transports two myce-
tangial fungi (Francke-Grosmann, 1963a, 1967; Gue
´rard
et al., 2000). Larval mines in phloem that is obviously dis-
colored by fungi are notably shorter than those in phloem
with no discoloration. When the fungus is clearly well estab-
lished, one can see that larvae double-back in their own
feeding tunnels and feed on the white fungus growing
on the tunnel walls; the first action of eclosed young adults
is to completely graze white fungal conidia and hyphae,
which have grown on the walls of their pupal chambers
(Kirkendall, unpubl.). Several unrelated North American
Ips species seem to have a similar biology (summarized in
Harrington, 2005). Tomicus minor is a common Eurasian
scolytine breeding in pine trunks and thicker branches; first
TABLE 3.2 Number of Scolytinae Genera and Tribes with at Least one Species Exhibiting the Given Larval Feeding
Mode (247 total genera, 26 total tribes)
Number of Taxa with at Least One Species Phl Xym Spm Myc Mye Xyl Hbv ?
Genera 121 63 9 2 14 21 17 31
Tribes 20 10 5 1 6 11 9 14
Some genera and tribes are represented in more than one category. Phl ¼phloeophagous (feeding in inner bark); Xym¼xylomycetophagous (ambrosia
beetles); Spm¼spermatophagous (feeding in seeds, fruits); Myc, mycophagous (feeding on non-symbiotic fungi); Mye¼myelophagous, feeding on pith;
Xyl¼xylophagous, feeding in sapwood; Hbv¼herbiphagous (herbivorous), feeding in non-woody plant tissues; “?,” unknown larval feeding habits. Data
from Appendix.
AB
CDE
FIGURE 3.5 Variation in gallery systems made by bark and
ambrosia beetles. (A, B, E) Engravings in phloem. (A, B) Cave-type
galleries of inbreeding polygynous species with communal larval feeding
for Dendroctonus micans (Kugelann) (from Chararas, 1962) and in
Hypothenemus colae (Schedl) (from Schedl, 1961b). (C, D) Ambrosia
beetle tunnel systems in sapwood for fungus cultivation for inbreeding
polygynous Xyleborus dispar (F.) and Xyleborinus saxeseni (Ratzeburg)
(from Balachowsky, 1949). (E) Monogynous egg tunnels of Kissophagus
granulatus Lepesme in Ficus (from Schedl, 1959).
96 Bark Beetles
and second instar larvae feed in inner bark, but later instars
move into the xylem where they become strict fungusfeeders
(Harrington, 2005). Both I. acuminatus and T. minor would
seem to be intermediate between true phloeophages and
obligate fungus feeders. They are both associated with
Ambrosiella fungi (as well as bluestain fungi), which are
ambrosia fungi in xylomycetophagous species.
The relationship of symbiotic fungi with certain species
of Dendroctonus and Ips is not an obligate one, but suc-
cessful establishment of their fungi definitely enhances larval
fitness in some species. Southern pine beetle (Dendroctonus
frontalis Zimmermann) larvae feeding in the absence of their
two mycetangial fungi have significantly reduced offspring
survivorship (Barras, 1973), and females breeding without
these mutualistic fungi lay only half as many eggs as controls
(Goldhammer et al.,1990). Similar fitness effects of mutual-
istic fungi are seen in the mountain pine beetle, D. pon-
derosae Hopkins (Six and Paine, 1998). Southern pine
beetle mutualistic fungi raise the nitrogen content of the
phloem and increase its digestibility (Ayres et al.,2000).
Fox et al. (1992) found evidence for enhanced growth of
Ips paraconfusus Lanier larvae when the associated fungus
was present in the phloem, and Yearian et al. (1972) found
that reproduction by females of I. avulsus (but not for two
other Ips species) is increased by the establishment of their
associated fungus. The terms “phloemycetophagous” and
“mycophloeophagous” have been suggested for inner bark-
breeding species that regularly feed on phloem plus fungus
(Kirisits, 2004; Six, 2012).
We have focused on fungi here, but the nutritional
quality of substrates consumed by bark beetles results from
a complex interaction between the physical and bio-
chemical attributes of the tissues consumed (Kirkendall,
1983; Haack and Slansky, 1987; Reid and Robb, 1999;
Six, 2012) and a complex community of fungi, yeasts, bac-
teria, and other microbes (Cardoza et al., 2006b; Hofstetter
et al., 2006; Six, 2012, 2013;Chapter 6).
3.2 Xylomycetophagy (Ambrosia Beetles)
The larvae and adults of xylomycetophagous species eat
cultivated fungi growing on woody tissues (Schedl, 1958;
Browne, 1961; S. L. Wood, 1982: see Box 3.1,Table 3.1,
and Figure 3.5C, D), and are referred to as ambrosia beetles
BOX 3.1 Terminology
Most specialized terms are defined in the text. However, there
are a few that are not, or that deserve special comment. We
largely follow well-established conventions in bark and
ambrosia beetle research (e.g., S. L. Wood, 1982), but have tried
to align terms regarding mating systems and social behavior
with the vocabulary being used more generally in behavioral
ecology (Wilson, 1975; Shuster and Wade, 2003).
Alloparental—Refers to parenting by individuals other than
the biological parents of the offspring, such as of ambrosia
beetle larvae by siblings or aunts.
Ambrosia beetles—Ambrosia beetles are those Scolytinae
(plus all Platypodinae) whose larvae feed primarily on co-
evolved symbiotic “ambrosia fungi,” which adult females
cultivate in tunnel systems in woody tissues. They may
consume wood in the process (xylomycetophagy sensu
Hulcr et al. in Chapter 2) or not (mycophagy sensu Hulcr
et al. in Chapter 2), but we will not make this distinction
(see also “xylomycetophagy,” below).
Bark—Shorthand for inner bark, the secondary phloem
tissue of woody dicots.
Bark beetles—In the literature, this term is used (confus-
ingly) in two senses, with three different meanings. Taxo-
nomically, “bark beetles” refers to the subfamily
Scolytinae; for clarity, we will avoid this usage. The
expression is used two ways in an ecological sense: it can
mean species breeding in inner bark (live and dead phloem
tissues), but many authors also use it in apposition to
ambrosia beetles (that is, to include all species that are
not xylomycetophagous). To avoid confusion, we will
mainly use “phloeophagous” to indicate Scolytinae that
breed in inner bark; occasionally, as in discussions primarily
focused on ambrosia beetles, we use bark beetles (or “non-
ambrosia beetles”) as an umbrella term for all feeding modes
other than xylomycetophagy. We will not use it
taxonomically.
Bark and ambrosia beetles—This expression is often used as
a collective term for Scolytinae. “Bark beetles,” in this
phrase, refers to all feeding modes other than obligate
fungus feeding. We use this compound phrase broadly, to
encompass both Scolytinae and Platypodinae, in order to
avoid the excessively long “bark and ambrosia beetles
and pinhole borers” when referring collectively to these
two lineages.
Declivity—The downward-sloping posterior portion of the
elytra: the back end of the beetle.
Frass—boring dust; the variegated mixture of feces and
wood bits (digested or not) resulting from the tunneling
activities of wood-boring insect larvae or adults.
Frons—Front of the head: the area between the eyes, from
the vertex (top of the head) to epistoma (upper margin of
the mandibles).
Hardwoods—Non-monocot angiosperm trees, as opposed
to conifers. We use “broadleaf trees” synonymously, though
technically this term also includes monocots.
Harem polygyny—Also known as simultaneous polygyny
(as opposed to serial polygyny) in anthropology and behav-
ioral ecology literature; in a harem polygynous scolytine, at
least some gallery systems have multiple females.
“Polygamy” (see below) is often used incorrectly as a
synonym.
Continued
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 397
(Schmidberger, 1836; Hubbard, 1897). Ambrosia beetles
actively cultivate coevolved mutualistic fungi. The fungus
forms layers of nutritious ambrosial growth within a few
days (Francke-Grosmann, 1967). This growth is pre-
dominantly composed of fruiting structures of a single
species of ascomycete fungus, which serves as major food
source for adults and larvae. These fungi typically grow as
mycelia, but form fruiting structures in the presence of the
tending beetles (Batra, 1967; French and Roeper, 1972a;
Biedermann, 2012).
Xylomycetophagy (cultivation of fungi growing in
wood) is found in 63 genera in 10 tribes of Scolytinae
(Table 3.2) and in all but the most basal Platypodinae.
Based on the most recent phylogenetic analyses (Jordal
and Cognato, 2012), it has evolved 10 or 11 times in Sco-
lytinae, depending on details of the analysis (Figure 3.4),
and it has originated once in Platypodinae (Jordal et al.,
2011). Two of these origins are recent, being single species
in large scolytine genera (Hypothenemus,Scolytodes).
Ambrosia beetles usually tunnel in sapwood or pith, but
some can breed in seeds, leafstalks, or the tissues of woody
monocots. Several corthyline ambrosia beetle species,
for example, have only been collected from the woody pet-
ioles of large, fallen Cecropia leaves (Wood, 1983, 2007;
Jordal and Kirkendall, 1998), which are also utilized by
generalist ambrosia beetles such as Xylosandrus morigerus
(Blandford) (Andersen et al., 2012) and X. crassiusculus
(Motschulsky) (Kirkendall and Ødegaard, 2007). All Platy-
podinae are tightly associated with fungi and usually col-
onize broadleaf trees; all but Schedlarius (xylophagous in
rotted wood) and Mecopelmus (phloeophagous) are
ambrosia beetles.
Most xylomycetophagous species transport their fungi
in mycetangia or the gut (Schneider-Orelli, 1911;
Francke-Grosmann, 1975). Vectoring of fungi within the
gut is probably the ancestral mode of spore transmission,
but still seems to be the dominant mechanism in some
ambrosia beetles, including examples of both Scolytinae
and Platypodinae that have no or reduced mycetangia. Xyle-
borinus saxesenii, for example, has very small elytral
BOX 3.1 Terminology—cont’d
Herbiphagy—Biologists often call feeding on any plant
tissue “herbivory.” Bark and ambrosia beetle researchers
use the related term “herbiphagy” for taxa feeding on fleshy
(not woody) plant tissues, such as plant leaves, leaf stalks, or
stems and branches of non-woody plants.
Monocots—Monocots are one of the two major groups of
flowering plants, the other being dicots. Monocots comprise
a monophyletic clade of plants that develop from a single
cotyledon; monocot host plants of bark and ambrosia
beetles include grasses (especially bamboos), palms,
agaves, lilies (Yucca trees), and orchids.
Mycophagy—Used by us in a very narrow sense, for feeding
on free-living fungi; other authors use this term broadly
for any form of feeding on fungal hyphae and conidia
(e.g., Harrington, 2005).
Monogyny—In monogynous species, only one female
breeds in a gallery system.
Parasitoids—Parasitoids are insects that live on or in their
hosts for some time before eventually killing them. Para-
sitoids of bark and ambrosia beetles are usually wasps, most
commonly chalcidoids, pteromaloids, proctotrupoids, or
ichneumonoids.
Pinhole borers—Currently, “pinhole borer” is often used to
refer to Platypodinae as a group, though in older literature it
may refer to any ambrosia beetle. “Shothole borer” has also
been used as a generic term for ambrosia beetles, though at
some point it seems to have been co-opted by North
American entomologists for the phloeophagous bark beetle
Scolytus rugulosus (Mu
¨ller), a minor pest of fruit trees.
Polygamy—Also known as communal breeding, colonial
breeding, or promiscuous breeding; in Scolytinae, a mating
system where several males and several females are
involved in constructing egg tunnel systems. In zoology,
usually refers to a mating system in which both sexes mate
with multiple partners, and have roughly equal variation in
mating success.
Spermatophagy—Used (only) by Scolytinae researchers to
classify species breeding in seeds and their encasing fruit
tissues, and the viviparous propagules of mangrove trees.
In the latter two cases, spermatophagy overlaps with herbi-
phagy, as the beetles are breeding in fleshy tissues. Other
biologists call insects breeding in seeds “seed predators”
or “seed parasites.” Outside of bark beetle research, the term
refers to phagocytosis of spermatozoa.
Xylomycetophagy—We use this term to refer collectively to
the feeding category for ambrosia beetles: taxa whose larvae
and adults feed primarily on cultivated co-evolved fungi.
We do not distinguish between fungus farming species that
do and do not ingest wood as well as fungus. Tunnel
elongation, egg niche enlargement, and construction of
pupal chambers (such as by all Platypodinae) may lead to
ingesting wood, and in some taxa, species may be con-
suming wood incidentally while feeding on mycelia. For
many ambrosia beetles, wood consumption is an aspect
of their feeding ecology that is simply unknown; if “xylomy-
cetophagy” is used narrowly to refer to ambrosia beetles
known to feed on wood as well as fungi, and “mycophagy”
used for taxa known to ingest fungi exclusively, then there
remains no formal term (of the sort “phloeophagy,” “xylo-
phagy,” etc.) to categorize feeding behavior of all ambrosia
beetles, or to refer to ambrosia beetles for which relevant
feeding behavior details are not known.
Xylophagy—Scolytinae that breed in tunnels in sapwood,
and do not cultivate fungi.
98 Bark Beetles
mycetangia (Francke-Grosmann, 1956a) and transmits its
principal ambrosial fungus via the gut (Francke-
Grosmann, 1975). In others like Anisandrus dispar (F.) with
well-developed mycetangia, mycetangia and gut may
harbor different fungi (see also X. saxesenii:Biedermann
et al., 2013); such redundancy may serve as an insurance
mechanism in case one of the organs is infected by para-
sites. However, some others lack mycetangia completely
because they rely on the fungal gardening of neighboring
beetles of other species.
Fungus stealing was suspected by Kalshoven (1960a)
and Beaver (1976), but was first thoroughly documented
by Hulcr and Cognato (2010), who termed it “myco-
cleptism.” The latter researchers found mycocleptism to
be the main foraging strategy for at least 16 species mainly
from the xyleborine genera Ambrosiophilus (eight species)
and Diuncus (five species), but also including Xylosandrus
hulcri Dole and Cognato, the scolytine Camptocerus
suturalis (F.), and one Platypodinae, Crossotarsus imitatrix
(Schedl). The “mycocleptae” tunnel close to the tunnel of
an established “provider” species, in some instances
breaking into the adjacent gallery system and destroying
neighboring brood. The walls of the mycocleptae’s tunnels
then begin to produce ambrosia fungus, which had been
introduced by the provider species. At least the genus
Diuncus has lost mycetangia all together, and is completely
dependent on this parasitic strategy.
3.3 Xylophagy (Breeding in Wood)
Species in which larvae feed wholly in sapwood occur in
only 21 genera spread among 11 tribes. The most
species-rich xylophagous lineage occurs in the Micracidini,
in which three genera of wood feeders, Hylocurus,
Micracis, and Thysanoes, include 119 species. Four Hyle-
sinini genera seem to be entirely xylophagous, Dactyli-
palpus,Hapalogenius,Phloeoborus and Rhopalopselion,
and Hylesinopsis partially so (see Appendix). The
remainder of xylophagous examples is single species or
small clades. Xylophagy has originated about nine times
(Figure 3.4; see the more detailed phylogeny in Jordal
and Cognato, 2012). Wood is nutritionally a very poor
resource for insects (Cowling and Merrill, 1966; Kramer
and Kozlowsky, 1979; Haack and Slansky, 1987). Many
organisms feeding on wood are known to be dependent
on the contributions of gut microbes. This has long been
suspected to be the case for xylophagous bark beetles as
well, but there has been relatively little research on this
aspect of their biology. Xylophagous species often have
low fecundity, relative to phloeophagous species
(Kirkendall, 1984). The primary benefit to adopting xylo-
phagy in these beetles would seem to be lower larval mor-
tality from predators and parasites, but it may also be
important that the physical environment (temperature,
wood moisture, food quality, persistence of resource
quality) is relatively stable, much more so than would be
expected for inner bark.
Browne (1961) treats pith and twig breeders as xylopha-
gous; we prefer to separate the two, since pith and sapwood
are considerably different in structure, density and
hardness, and possibly in nutritional quality, though levels
of nitrogen are roughly similar (Cowling and Merrill, 1966;
Kramer and Kozlowsky, 1979).
3.3.1 Breeding in Wood Nutritionally
Improved by Fungi
Currently, this is a hypothetical group, as no wood-breeding
scolytines have been studied in any detail. The xylophagous
genera Dactylipalpus and Phloeoborus have distinctive
mycetangia, but do not appear to be true ambrosia beetles.
Beaver and L€
oyttyniemi (1985) report that Dactylipalpus
camerunus Hagedorn is polyphagous, monogynous, and
xylophagous, and attacks moderate to large logs and dying
or dead stems. Females have pronotal mycetangia, sug-
gesting that they may be closely associated with fungi. In
addition, Browne (1963) reports Dactylipalpus as xyloph-
agous. Similarly, as far as is known, Phloeoborus are
xylophagous, but females have mycetangia (Wood, 1986).
3.4 Herbiphagy
Some genera or single species breed in herbaceous plant
tissues, and are classified as herbiphagous (Box 3.1,
Table 3.1). It is a rare feeding strategy in Scolytinae, being
found in only 17 genera (6%) in nine tribes (Table 3.2), and
has evolved only about eight times (Figure 3.4). Half of the
genera in which herbiphagy is represented are specialized to
this lifestyle (Appendix). One radiation in the Dryocoetini
accounts for about two-thirds of all herbiphagous species.
Feeding habits in this category include breeding in her-
baceous plants, ivy, Clematis, grass stems including
bamboos, cacti and succulent euphorbs, leaf petioles, and
the viviparous propagules of mangrove trees. We include
here two species that breed in roots of herbaceous plants:
(1) Hylastinus obscurus (Marsham) is a minor pest of clover
in North America, where it is an introduced species, though
there are no records of it breeding in clover from Europe
where it is native (Webster, 1910; Koehler et al., 1961);
and (2) the recently discovered Dryocoetes krivolutzkajae
Mandelshtam, which breeds in roots of Rhodiola rosea
(Crassulaceae), the only bark beetle of treeless tundra land-
scapes (Mandelshtam, 2001; Smetanin, 2013). And we
include the only galling bark beetle, Scolytodes ageratinae
Wood, which attacks live plants of a herbaceous montane
species of Ageratina (Asteraceae) in Costa Rica (Wood,
2007; Kirkendall, unpubl.; see Section 3.9)
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 399
Thamnurgus is a typical example of a herbiphagous
genus. Thamnurgus euphorbiae Ku
¨ster has been approved
for biological control of Euphorbia esula L. (leafy spurge),
an invasive weed in the USA (Campobasso et al., 2004).
Females oviposit in the stem, starting at the top of the
plants. Apparently, females have high lifetime fecundity
(88 eggs) but lay relatively few eggs per plant. Colonized
plants are weakened structurally and break easily, pro-
ducing fewer seeds. Thamnurgus pegani Eggers breeds in
stems of Peganum harmala L. (Nitrariaceae), a perennial
plant toxic to grazing animals (Gu
¨clu
¨and €
Ozbek, 2007).
One or a few eggs are laid between the stem and a lateral
branch junction, and larvae tunnel down the inside of the
stem in the pith. The tissue on which larvae are feeding
becomes blackish-brown due to presence of Fusarium oxy-
sporum Schltdl.; the fungus was also isolated from the
bodies of the bark beetles. A couple of weeks after eggs
are laid, larval tunnels are still very short (6 mm); this
and the presence of white mycelia on the surface of the
stained pith tissues suggest that the species may be gaining
significant nutrition from the fungus.
An entire scolytine community (29 species, six genera,
three tribes) can be found in the cactus-like, shrubby, and
tree-like euphorbs of the Canary Islands, Madeira, Cape
Verde, and North Africa (Jordal, 2006). Species are nar-
rowly host specific, but up to half a dozen species could
be found in one branch. Like the Thamnurgus mentioned
above, these herbiphagous species are characterized by
unusually low (within-plant) fecundity, though they likely
oviposit in several plants. The scolytines breed only in dead
branches and twigs, but differ ecologically in moisture pref-
erences and host diameter.
The seeds of some mangrove trees (like those of Rhizo-
phora or Bruguiera) grow while still on the mother plant;
these viviparous propagules later drop from the tree and float
until they strand on muddy sediments, after which they begin
to root. Coccotrypes species breeding in the propagules of
mangrove trees are sometimes categorized as spermato-
phagous, but we classify them here as herbiphagous since
they are actually breeding in live, non-ligneous (not woody)
plant tissues and not in seeds or fruit tissues. Hanging
or (usually) newly beached seedlings are attacked by Cocco-
trypes rhizophorae (Hopkins), C. fallax (Eggers), and
C. littoralis (Beeson) (Beeson, 1939, 1941; Kalshoven,
1958; Browne, 1961). These species specialize in man-
groves, as opposed to most Coccotrypes, which are host gen-
eralists and breed in seeds, bark, or leafstalks with some,
such as C. cyperi (Beeson), breeding on all three. The man-
grove Coccotrypes are not found in other hosts, or in
branches or trunks of mangroves. Interpreting this feeding
behavior as herbaceous gets some support from the obser-
vation that C. rhizophorae also attacks the soft, growing tips
of aerial roots of Rhizophora mangle L.; it does not,
however, breed in the older, woody portions of the roots
(Aktinson and Equihua-Martı
´nez, 1985b). In Neotropical
mangroves, only C. rhizophorae is found; it occurs in man-
grove forests throughout the world, and may have dispersed
to the New World on its own, as have the mangrove species
in these forests (Atkinson and Peck, 1994). Little has
been published on the biology of mangrove Coccotrypes,
but there have been two ecological studies of the effects of
C. rhizophorae in the Neotropics, where it seems that the high
levels of propagule attacks can have significant effects on the
mangrove ecosystem (Rabinowitz, 1977; Sousa et al.,2003).
Herbiphagy is a difficult category to define precisely,
especially without detailed knowledge of plant anatomy.
Dendrocranulus, for example, breeds in stems of cucurbit
vines. We choose to classify Dendrocranulus as myelo-
phagous (as do Atkinson and Peck, 1994) but it could also
have been classified as herbiphagous. Which is more
important physiologically, ecologically, and evolution-
arily? That it breeds in non-woody plants (herbiphagous),
or that it colonizes pithy tissues (myelophagous)? Petioles,
too, are problematic. Those of large fallen Cecropia leaves
are very woody, at one extreme, in contrast to those of
Gunnera, which although stiff, are quite moist and rather
fleshy (Figure 3.6). Scolytodes, a large neotropical genus
comprised primarily of phloeophagous and myelophagous
species, has radiated into both.
Lineages moving from bark to herbaceous tissues
probably are moving to food with similar or even higher
nutritional quality (with the exception of petioles: Jordal
and Kirkendall, 1998), but herbaceous tissues differ from
those of trees and woody shrubs tissues in their anatomy,
biochemistry, and especially in moisture content. The distri-
bution of herbiphagy in Scolytinae, and what we know of the
biology of herbiphagous species, suggest that adopting her-
biphagy is not readily accomplished and demands a suite of
new adaptations (including major life history adjustments),
though perhaps less so in those cases that most resemble
woody branches (such as the highly lignified petioles of
Cecropia leaves).
FIGURE 3.6 An example of herbiphagy: cave-type egg gallery of Scoly-
todes gunnerae Wood in live fleshy leafstalk of Gunnera insignis in Costa
Rica. Eggs are laid loose in the gallery; the leafstalk is ca. 3 cm in diameter.
100 Bark Beetles
3.5 Myelophagy (Pith Breeders)
Pith breeding is very uncommon in Scolytinae. Only 14
genera in six tribes have species that regularly breed in pith
(Table 3.2). Pith is composed of undifferentiated paren-
chyma cells, which function in storage of nutrients, and
in eudicots is located in the center of the stem. It is mainly
present in young growth; in older branches and stems it is
often replaced by woodier xylem cells. Pith is poor in
nutrients, being about equivalent to young sapwood in
terms of nitrogen content (Cowling and Merrill, 1966)or
somewhere in between sapwood and inner bark (Haack
and Slansky, 1987). It is, however, easy to tunnel through.
This combination of features is illustrated by the breeding
biology of Scolytodes atratus Wood and Bright in Cecropia
petioles, the centers of which are composed of a relatively
large cylinder of soft white pith: tunnels can be several tens
of cm in length yet produce only four or five offspring
(Wood, 1983; Jordal and Kirkendall, 1998).
Typically, pith breeders construct irregular chambers or
meandering egg tunnels, often going both up and down the
twig from the entrance. Twig breeders are generally mono-
gynous, even in otherwise harem polygynous genera such as
Pityophthorus,Araptus,orScolytodes (Kirkendall, 1983).
Twigs of many woody plants are largely pith, so twig
breeders are classified as myelophagous; often, an entire
twig is hollowed out by adult and larval feeding, but most
of the tissue consumed is pith. There are a handful of
Pityophthorus species that breed mainly or only in twigs
and that are categorized here as myelophagous. In tropical
hardwoods, the tribe Bothrosternini comprises mainly
pith borers (some Cnesinus are phloeophagous), some of
which have evolved fungus farming in pith (Beaver,
1973;S. L. Wood, 1982, 2007;Kolarik and Kirkendall,
2010;Section 3.2,Appendix).
3.6 Spermatophagy (Seed Breeders)
Spermatophagy (or spermophagy) as used by bark beetle
researchers denotes species breeding in seeds and the
surrounding fruit tissues. This term has been applied very
broadly to encompass true seed predators (Janzen, 1971)
but also species collected from fleshy fruits, woody
seedpods, mangrove propagules (which we treat as herbi-
phagous), or cones (Schedl, 1958; Browne, 1961;S. L.
Wood, 1982, 2007;Kirkendall, 1983; Atkinson and
Equihua-Martı
´nez, 1986b). As such, the category is rather
heterogeneous with respect to actual feeding adaptations.
Normally, exposed seeds from fallen fruits (or defecated
seeds) are preferred both by seed specialists and by
generalists when they breed in seeds.
Nine genera in five tribes have spermatophagous
species, and true seed breeding has originated at least eight
times (Table 3.2;Figure 3.4). Two genera of Scolytinae
only breed in seeds (Pagiocerus, neotropical, five species;
Dactylotrypes, one species endemic to the Canary Islands),
as does possibly Spermophthorus (Wood, 2007).
3.6.1 Pagiocerus
Pagiocerus frontalis (F.), found in Central and South
America, is often collected from seeds of Lauraceae,
including commercial avocado (Persea americana Mill.).
In Mexico, it bores into partially or completely exposed
seeds lying on the ground and does not attack fruits on the
tree (Atkinson and Equihua-Martı
´nez, 1985b; Atkinson
et al., 1986). In South America, it has been recorded as a pest
of maize since at least 1930; the seeds are attacked on the
plant and in storage, and it has been collected from coffee
berries in Ecuador (Yust, 1957; Okello et al., 1996b;
Gianoli et al., 2006). In the laboratory, it can be bred on
cassava chips as well as maize (Okello et al., 1996a). The
biology of other Pagiocerus species is not known, except
that P. punctatus Eggers has been collected from male
strobili of Araucaria angustifolia (Bertol.) Kuntze in Brazil
(Mecke and Galileo, 2004).
3.6.2 Coccotrypes
Many species of Coccotrypes breed in small hard seeds,
especially palms. Most Coccotrypes that breed in seeds also
breed in bark, leafstalks, or other tissues, but some are
known to be seed specialists (e.g., C. carphophagus
(Hornung), C. dactyliperda F.), and there are many species
that are not often collected but have only been found in seeds
(Beeson, 1939, 1941; Browne, 1962). Coccotrypes only col-
onize seeds that have fallen, i.e., seeds that are at least partly
exposed or completely bare of fruit tissues. Within seeds,
beetles experience similar selective pressures as many
ambrosia beetles (e.g., Xyleborini) by inhabiting a “bonanza
type” resource that is protectable and may provide ample
food for several offspring generations. Hence, this habitat
favors the evolution of inbreeding, biased sex ratios, dis-
persal polymorphism, and advanced social behavior
(Hamilton, 1978, 1979), which characterizes Coccotrypes
(Herfs, 1950; 1959; Gottlieb et al., 2014) and many
Hypothenemus species (see below) as well as Xyleborini.
3.6.3 Other Seed Breeders
Most Araptus species are phloeophagous or myelophagous,
but at least 19 species breed in seeds (S. L. Wood, 1982,
2007); half of these are apparently legume seed specialists.
Most Hypothenemus are highly polyphagous, but a few reg-
ularly or most commonly breed in seeds (Beeson, 1941;
Browne, 1961;S. L. Wood, 1982, 2007;Atkinson and
Equihua-Martı
´nez, 1985c;Chapter 11) and a few species
in other genera at least sometimes breed in seeds (see
Appendix). In addition, species of Conophthorus that breed
in developing cones of Pinaceae are also classified as
spermatophagous.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3101
3.6.4 Economically Significant Seed Breeders
Only one example of a spermatophagous species attac-
king fruits still on the plant is known to us: the coffee berry
borer, Hypothenemus hampei (Ferrari) (Chapter 11). The
coffee berry borer is the most serious pest of coffee in most
coffee growing countries (LePelley, 1968; Benavides et al.,
2005; Jaramillo et al., 2006;Chapter 11). It attacks healthy
coffee berries, and breeds in the developing endosperm.
This is the only example known to us of scolytines attacking
live, attached fruits, and is by far the most economically
important spermatophage and the most widely known
tropical bark beetle. The congeneric tropical nut borer
(Hypothenemus obscurus (F.)) is a pest of macadamia in
Hawaii and Australia (Jones, 1992; Delate, 1994;
Mitchell and Maddox, 2010;Chapter 11). It breeds in both
seeds and bark, but primarily breeds in seeds and nuts of a
wide variety of plants (S. L. Wood, 1982, 2007).
3.6.5 Cone Breeders
Conophthorus (Chapter 12) have the unique habit of
breeding in the developing cones of gymnosperms
(Miller, 1915; Lyons, 1956; Chamberlin, 1958; Keen,
1958; Ruckes, 1963; Hedlin et al., 1980; Flores and
Bright, 1987;Furniss, 1997). Females bore in from the base
of a developing cone, severing the conductive tissues and
killing the cone whether or not brood is successfully pro-
duced (Ruckes, 1963; Godwin and Odell, 1965; Hedlin
et al., 1980). Seed crop loss to Conophthorus species can
be over 50% (Cognato et al., 2005). Conifer seeds are par-
ticularly high in nitrogen, higher than bark (Kramer and
Kozlowsky, 1979). Conophthorus are relatively host spe-
cific; each species breeds in one Pinus host, or in a few
closely related Pinus species (Hedlin et al., 1980;
Cognato et al., 2005). Conophthorus ponderosae, the one
species that is recorded from many pine host species,
may be a species complex (Cognato et al., 2005; but see
Menard and Cognato, 2007).
Curiously, regular breeding in gymnosperm cones has
evolved only once, in North America (Cognato et al.,
2005). Conophthorus has likely evolved from a
Pityophthorus ancestor such as the closely related
P. schwerdtfergeri (Schedl), which breeds in both twigs
and cones (Cognato et al., 2005). It should be noted that
some Conophthorus feed on shoots, e.g., C. coniperda
Schwarz, especially when all cones are occupied (Morgan
and Mailu, 1976), and C. resinosae Hopkins both feeds
and breeds in shoots as well as cones (McPherson et al.,
1970; de Groot and Borden, 1992). Additionally, several
Pityophthorus species have been collected from cones in
North America (Godwin and Odell, 1965). Given these
facts, it seems odd that the habit has not also evolved in
Eurasian conifer scolytines.
3.7 Mycophagy (Fungus Feeders)
Other than galling (one species), mycophagy is the rarest
feeding mode in Scolytinae, known from only two genera
in two tribes. At least some species in the rarely collected
genus Trischidias breed in the fruiting bodies of asco-
mycete fungus growing in dead twigs or wood (Deyrup,
1987). Similarly, the rare Lymantor decipiens (LeConte)
(but not other Lymantor) is found in dry sapwood with black
fungi, upon which they are thought to feed (Swaine, 1918;
Blackman, 1922;S. L. Wood, 1982; Kirkendall, unpubl.).
3.8 Breeding in Monocots
Interestingly, there are only a few host-specific phloeo-
phages breeding regularly in the outer tissues of monocots,
and there seem to be relatively few records of polyphagous
ambrosia beetles breeding in woody monocots. Generally,
for bark and ambrosia beetles, the preferred tissues of
woody plants are the vascular tissues: cambium plus
phloem for phloeophages, and xylem for xylophages and
most ambrosia beetles. The vascular tissues taken together
constitute a thick cylinder in gymnosperm trees and dicot
angiosperms. In monocot angiosperms, xylem and phloem
occur together in small bundles scattered in a matrix of
nutrient-poor ground tissue. Thus, in monocots, there are
no thick rings of relatively favorable tissue for phloeo-
phages as there are in dicots and gymnosperms. It may also
be that this radically different distribution of vascular
tissues precludes normal phloeophagous gallery con-
struction by bark beetles, and may also hinder normal
fungus development in ambrosia beetles. Monocot spe-
cialists include few species of Chramesus (a genus with
phloeophagous and xylophagous species) and of Corthylus
(ambrosia beetles) that breed in native bamboos in the neo-
tropics (S. L. Wood, 1982, 2007;Atkinson and Equihua-
Martı
´nez, 1986b). Otherwise, breeding by non-ambrosia
beetle scolytines in monocots is restricted to leaves of
yuccas and agaves (species of Chramesus, Cactopinus,
Pseudothysanoes,Hypothenemus:Atkinson and Equihua-
Martı
´nez, 1985a, b, c; Atkinson, 2010) and stems, pseudo-
bulbs, or flowering stalks of bromeliads and orchids
(Chramesus annectans (Wood), Atkinson et al., 1986;Tri-
colus coloreus Wood, an ambrosia beetle, Wood, 2007;
Xylosandrus ambrosia beetles, Reitter, 1916, Dekle and
Kuitert, 1968, and Dole et al., 2010). In addition, several
Hypothenemus species and Chramesus exilis Wood breed
in woody Smilax vines (Atkinson and Equihua-Martı
´nez,
1985a, b); Hypothenemus pubescens (Hopkins) breeds in
the stems of grasses (S. L. Wood, 1982;Atkinson and
Peck, 1994). With the exception of the Hypothenemus
and Xylosandrus ambrosia beetles, all of these seem to be
monocot specialists, though some are rarely collected, so
102 Bark Beetles
their true host breadth is not known. Trunks and woody
parts of palm leaves are colonized by generalist (polyph-
agous) ambrosia beetles, but the species richness of
ambrosia beetles in palms seems to be much lower than that
in dicots in the same forests. Sufficiently large, hard
monocot seeds, on the other hand, which have similar
structure to those of angiosperms, are readily colonized
by both seed specialists and seed generalists.
3.9 Breeding in Live Hosts
Although bark and ambrosia beetles are primarily adapted
to colonizing recently dead woody plants, many lineages
have evolved to find and breed in living tissues. For species
feeding directly on plant tissues (not cultivating fungi),
living resources have the advantages of being generally
more nutritious than dead tissues, and may have fewer intra-
specific and interspecific competitors. Older dead resource
units may also have experienced a buildup of predators, par-
asites, and potentially hostile microbes. The disadvantages
of breeding in live resources are that they not only have an
array of preformed anatomical and chemical defenses but
can also mobilize further physical and chemical weapons.
In this section, we present information on Scolytinae and
Platypodinae that can tackle living tissues, e.g., wood,
seeds, or seedlings. We discuss tree killing, but not the mass
attacks on conifers by Dendroctonus or Ips, which are
covered in Chapters 8 and 9, respectively, or in other recent
works (Raffa et al., 2008; Kausrud et al., 2011, 2012;
Lindgren and Raffa, 2013). We will focus instead on the
less well-known instances of bark and ambrosia beetles
killing hardwoods or breeding in living plant parts.
Insects breeding in live as opposed to dead plant tissues
must adapt to active plant defenses. A clear consequence is
that those regularly colonizing living tissues are more host
specific than species breeding in the same tissue type but
only in dead tissues. Coccotrypes and Hypothenemus,
which breed in seeds, attack seeds of many plant families
as long as they are big enough and hard enough (Browne,
1961; Schedl, 1960b, 1961). Coccotrypes breeding in man-
grove propagules do not breed in any other hosts, or even in
branches or trunks of mangrove trees. Hypothenemus
hampei is the only Hypothenemus species that can breed
in developing Coffea seeds, though many other species have
been collected from Coffea trees; interestingly, it has been
collected from hard seeds and woody pods produced by
plants of several different families, but the only live fruits
it is known to regularly colonize are those of Coffea
(Schedl, 1960b, 1961; Vega et al., 2012). A very few
ambrosia beetles are known only to attack standing,
live trees, and in each case they are unusually host specific.
The rare species Xyleborus vochysiae Kirkendall has
only been collected from one host species (see below), in
contrast to other tropical Xyleborus, which usually can be
found in dead hosts of several to many different plant fam-
ilies. Three platypodine ambrosia beetles breed exclusively
in live trees. The West African Trachyostus ghanaensis
Schedl breeds only in Triplochiton scleroxylon K. Schum.
(Sterculiaceae) (Roberts, 1960), while the Malayan Den-
droplatypus impar (Schedl) breeds only in the certain
Shorea species (Dipterocarpaceae) (Browne, 1965). The
Australian A. incompertus is restricted to one genus, Euca-
lyptus (Kent, 2002). As with Xyleborus, platypodine
ambrosia beetles are usually quite polyphagous. Another
West African platypodine, Doliopygus dubius (Sampson),
is polyphagous when colonizing felled trees and logs, but
attacks live (apparently healthy) trees of only one species,
Terminalia superba Engls. and Diels (Combretaceae)
(Browne, 1961). There is one exception to this trend,
however. Corthylus columbianus Hopkins breeds in live
trees, but does not seem to be very host specific (Crozier
and Giese, 1967a, b).
3.9.1 Killing Entire Trees
Relatively few bark and ambrosia beetles are able to col-
onize and kill entire trees, but those that do can have major
ecological and economic impacts. Species of Dendroctonus
(Chapter 8) and Ips (Chapter 9), in particular, kill millions
of trees each year in North America, Europe, and Asia.
Given the worldwide local and regional importance of tree
killing by Dendroctonus and Ips, there is an erroneous but
widespread notion that tree killing is by and large restricted
to Pinaceae, as reflected in the title of a paper by the
Australian forest entomologist Clifford P. Ohmart, who
asks “Why are there so few tree-killing bark beetles asso-
ciated with angiosperms?” (Ohmart, 1989). The article’s
claim, that the ability to kill trees has only evolved in taxa
breeding in Pinaceae, seems to have been accepted uncrit-
ically in the few papers citing this work (e.g., Hulcr and
Dunn, 2011). Ohmart (1989) argues for a key difference
in how angiosperm vs. conifer host trees react physiologi-
cally to beetle attack. However, the article is flawed by a
bias towards temperate (primarily North American) Scoly-
tinae; this bias is frequently encountered in discussions of
bark and ambrosia beetles by forest entomologists (e.g.,
Stark, 1982). Ohmart’s (1989) hypothesis depends on
assumptions about differences in temperate vs. tropical sco-
lytine–host tree interactions, but not one article on tropical
scolytine biology is cited.
The main tree-killing bark beetle in Europe is Ips typo-
graphus L., which breeds in spruce (Picea), but it is never-
theless not clearly a primary attacker. It mainly kills healthy
trees during irregular outbreaks triggered by massive
population buildups; otherwise, it kills trees that are
highly stressed or attacks recently dead and dying trees
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3103
(Berryman, 1982; Kausrud et al., 2012;Chapter 9). Sphaer-
otrypes hagedorni Eggers (Diamerini) can kill its savannah
host tree Anogeissus leiocarpus (DC.) Guill. and Perr.
(Combretaceae), but does so only in the dry season, when
trees are water stressed; attacks on living trees in the wet
season fail due to active tree defenses, i.e., gum exudation
(Roberts, 1969).
A century ago, the hickory bark beetle Scolytus quadris-
pinosus Say was a focus of attention by forest entomolo-
gists. It was causing huge losses of hickory timber,
particularly trees under moisture stress, in the eastern
USA (Schwarz, 1901; Hopkins, 1904, 1908; Blackman,
1924; Blackman and Stage, 1924; Beal and Massey,
1945). During periods of drought, this species kills large
tracts of hickory trees in the eastern USA. Normally, it
attacks only weakened trees; galleries started in vigorous
trees soon fill with sap, and fail (Blackman, 1924;
Blackman and Stage, 1924). Felt (1914) and Blackman
(1924) used precipitation data to show that significant tree
killing only occurred in years with deficiencies of rainfall.
Early in the 20th century, S. rugulosus was reported to
be regularly killing “large numbers” of scrubby wild plum
(Prunus serotina Ehrh.), with highest densities on trees
injured by ground fires used to clear weeds (Blackman,
1922). Normally, these bark beetles colonize injured
branches or trunks, but when numerous they attack healthy
hosts (Blackman, 1922; Beal and Massey, 1945). Orchard
practices have since changed considerably, and S. rugulosus
is no longer considered an important pest of Prunus
fruit trees.
Similarly, the peach bark beetle Phloeotribus liminaris
(Harris) was studied in the early 1900s because it was dam-
aging and even killing peach, black cherry, wild cherry
trees, and mulberry in the northeast USA (Wilson, 1909;
Beal and Massey, 1945). Though it was originally collected
and described because of its association with “peach
yellows” in the 1850s (Harris, 1852), it was not considered
an economic problem until the turn of the century, when
plantings of peach and cherry had grown (Wilson, 1909).
Population buildups due to breeding in slash or windthrown
trees can lead to massive attacks on healthy trees during
breeding, but normally the main damage is due to gum
spotting (gumosis), the result of the tree’s reaction to
beetles overwintering under the bark in healthy tissues
(Beal and Massey, 1945); gum spot defects reduce the
veneer value of black cherry by 50–90% (Hanavan et al.,
2012). Beetles tunneling in healthy trees usually are either
pitched out or killed by the gum reaction (Rexrode, 1982).
These are just a few of many examples of phloeo-
phagous bark beetles locally killing native or ornamental
trees, regularly or in occasional outbreaks. A few hardwood
examples not yet mentioned include species of Alniphagus
aspericollis (LeConte) killing alders (Chamberlin, 1958;
Borden, 1969); Dryocoetes betulae Hopkins killing birches
(Hopkins, 1904); four Phloeotribus species that can occa-
sionally kill Prunus trees (Blackman, 1922; Atkinson and
Equihua-Martı
´nez, 1985a; Atkinson et al., 1986); Scoly-
todes guyanensis Schedl killing thousands of mahogany
trees “of all sizes” (Swietenia) in plantations (Gruner,
1974); Scolytus ratzeburgi Jansen killing birches (Tredl,
1915); and Taphrorhychus villifrons Dufour killing
dwarfed oaks (“nains”; Balachowsky, 1949).
Ambrosia beetles, too, occasionally or regularly attack
and kill live hardwood trees. The newly described xyle-
borine ambrosia beetle Coptoborus ochromactonus Smith
and Cognato was discovered and named because it was
killing large proportions of young trees in commercial balsa
plantations in Ecuador (Stilwell et al., 2014). Most mor-
tality occurred in the dry season and to the smallest trees;
deaths were attributed to the establishment of the beetles’
primary ambrosia fungus, a Fusarium (Stilwell et al.,
2014). A few ambrosia beetle species such as this one
can colonize live trees, though usually hosts are stressed
or diseased. If their ambrosia fungus thrives in live trees,
when density of attacks is high enough, the fungus’s rapid
spread in xylem tissues can disable water conduction and
effectively throttle the host. In a similar fashion, laurel wilt
disease is caused by the symbiotic Raffaelea fungus of the
Asian ambrosia beetle Xyleborus glabratus Eichhoff, which
is called the redbay ambrosia beetle in the USA. Laurel wilt
disease is killing thousands of mature forest, ornamental,
and plantation trees in the family Lauraceae (particularly
redbay Persea borbonia (L.) Spreng. and sassafras, Sas-
safras albidum (Nutt.) Nees) and is a potential threat to
two endangered species and to the southeastern US avocado
industry (Fraedrich et al., 2008; Hanula et al., 2008).
Other examples of ambrosia beetles killing hardwoods
include Xylosandrus germanus (Blandford) (oaks:
Heidenreich, 1960); Xyloterinus politus Say (birches:
Schwartz, 1891); Euplatypus parallelus (F.) (Beaver,
2013); Platypus quercivorus (Murayama) (oaks: Kamata
et al., 2002); Platypus subgranosus Schedl (Nothofagus:
Howard, 1973); and Euplatypus hintzi (Schaufuss)
(Eucalyptus in plantations: Roberts, 1969).
A few examples of gymnosperms being killed by oth-
erwise innocuous species include Pseudohylesinus grandis
Swaine, which normally breeds in weakened or dying
Douglas-fir but occasionally attacks and kills “a consid-
erable quantity of young timber” (Chamberlin, 1918); and
Phloeosinus rubundicollis Swaine, which has been
observed killing thousands of ornamental Chamaecyparis
(Chamberlin, 1958).
Some species that are considered harmless in their
native ecosystems (“secondary”) become deadly when
introduced to naive forests (Ku
¨hnholz et al., 2001; Ploetz
et al., 2013). Dendroctonus valens LeConte females breed
singly or in small numbers at the bases and in the roots of
pines, and attacks by this species have no impact on trees in
104 Bark Beetles
their native forests in North America. Meanwhile, in China,
where the species has recently become established, it kills
thousands of pines each year (Yan et al., 2005; Sun et al.,
2013;Chapter 8). Similarly, the secondary North American
bark beetle Ips grandicollis (Eichhoff) is a lethal pest of
exotic Pinus resinosa in plantations in Australia
(Morgan, 1967).
Considering these examples, it is important to be cau-
tious in concluding that only certain bark beetle species have
evolved to kill trees, or that bark and ambrosia beetles only
kill Pinaceae (Ohmart, 1989). While a handful of notorious
Dendroctonus species are specialists at tree killing, there is a
continuum of aggressiveness in Scolytinae and Platypo-
dinae, from species that only breed in live tissues to species
that come to a tree months after its death. Many species can
and do kill their hosts under the right conditions, even per-
fectly healthy individuals. In many of the examples cited
above, the individual trees that were killed were known or
suspected to be stressed. The point is, however, that these
trees would likely have survived had the above-mentioned
bark or ambrosia beetles not colonized them.
While the greatest ecological and economic impacts of
tree killing are by Dendroctonus species in low diversity,
widespread conifer forests, there is a large and growing
number of instances of serious tree pathogens vectored
by Scolytinae and Platypodinae in forests around the world,
primarily involving angiosperm hosts (Hulcr and Dunn,
2011; Ploetz et al., 2013). There has been considerable
research into a few examples, such as Dutch elm disease,
vectored in North America by both the native elm bark
beetle Hylurgopinus rufipes (Eichhoff) and the invasive
Scolytus multistriatus (Marsham), and in Europe by several
native species of Scolytus. Other cases, many of which are
only recently documented, are just beginning to be investi-
gated (Hulcr and Dunn, 2011; Ploetz et al., 2013). The
impacts of attacks by these beetle–fungus partnerships vary
from mild economic losses due to wood discoloration to
major ecological and economic consequences due to
massive tree mortality, mainly mortality of angiosperms,
contra Ohmart (1989).
3.9.2 Killing Plant Parts, Seedlings, and Seeds
Much less appreciated are the impacts of perhaps hundreds
of species, which affect live host plants in more subtle ways,
by killing branches or twigs, patches of bark, seedlings, or
seeds (Blackman 1922; Beeson, 1941; Chamberlin 1958;
Browne, 1961;S. L. Wood, 1982;Postner, 1974). These
bark beetles can nonetheless significantly reduce the
growth and reproduction of their hosts and repeated branch
killing can lead to death of entire trees.
A number of phloeophagous Scolytinae have been
described as progressive branch killers. Several ash bark
beetle species (Hylesinus) kill branches year after year,
eventually moving onto the trunk, perhaps because branch
losses have crippled the tree’s defenses (Doane, 1923;
McKnight and Aarhus, 1973; Postner, 1974; Gast et al.,
1989). Progressive branch killing has also been reported
for Hylesinus oleiperda F. in olive trees and ashes
(Postner, 1974; Graf, 1977), S. ratzeburgi in birches
(Tredl, 1915), and Pityophthorus costatulus Wood in The-
vetia (Apocynaceae) (Atkinson et al., 1986a), to give just a
few examples.
A few bark beetles that attack branches have been
researched because the damage they cause is of sufficient
economic import to warrant attention. The ambrosia beetle
known now as the black twig borer, Xylosandrus compactus
(Eichhoff), is well known as a pest of coffee and cocoa in
West Africa, and tea in Asia (Kalshoven, 1925; Brader,
1964; Kaneko et al., 1965; Entwistle, 1972), and where
introduced is a pest of a wide variety of ornamental and
native trees (Kalshoven, 1958; Browne, 1961, 1968;
Beaver, 1988; Chong et al., 2009). The adults bore into
healthy young stems, branches or twigs; concentrated
attacks can lead to death of the plant (Brader, 1964). Sadly
for coffee aficionados, the black twig borer is a major
impediment to coffee production in the Kona region of
Hawaii (Greco and Wright, 2013.)
A palearctic phloeophagous species reproducing
harmlessly in trunks of dead or dying pines is Tomicus
piniperda (L.) (Chapter 10). Like most other Tomicus
(Kirkendall et al., 2008), its impact is due not to its breeding
habits, but rather to the behavior of recently emerged young
adults, which feed in the pith of healthy tree tops and branch
tips (maturation feeding), killing them (Chararas, 1962;
La
˚ngstr€
om, 1983; La
˚ngstr€
om and Hellqvist, 1993;
Amezaga, 1997). Shoot pruning by T. piniperda in Nordic
pine forests has been estimated to reduce forest productivity
by up to 45% of the annual volume growth (Eidmann,
1992). Maturation feeding is especially intense in the
Chinese Tomicus yunnanensis Kirkendall and Faccoli,
and trees are so weakened by it that they can later be
attacked and killed by this species (Ye, 1997; Ye and
Ding, 1999; Lieutier et al., 2003).
A number of phloeophagous and myelophagous species
have evolved to breed in small plant parts incapable of
defending themselves (such as the Tomicus described
above). These species either tolerate local host defenses,
or can mechanically disable or overwhelm them. Whether
or not microbes are an important weapon (as they clearly
are in almost all tree killers) is not generally known but
is to be expected.
Pityophthorus puberulus (LeConte) offers an example
of apparent tolerance. Females breeding in terminal twigs
can be seen to be practically swimming in resin, and use
a mixture of frass and resin to plug the entrance (males
being absent in this parthenogenetic species) (Deyrup
and Kirkendall, 1983; Kirkendall, unpubl.). At least several
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3105
Pityophthorus species originally described in Myeloborus
seem to have the same biology, breeding in and killing
pitchy twigs of pine trees (Blackman, 1928).
The monogynous ambrosia beetle Corthylus punctatis-
simus (Zimmermann) girdles stems and roots of saplings of
a wide variety of angiosperm trees in eastern North America
(Merriam, 1883; Schwarz, 1891; Roeper et al., 1987a, b).
At high population densities, such girdling could have sig-
nificant ecological effects: as recounted by Merriam
(1883):“...in Lewis county [New York, USA] alone hun-
dreds of thousands of young sugar maples perished from the
ravages of this Scolytid during the summer of 1882.”
However, Schwarz (1891) commented that C. punctatis-
simus pairs destroy the underground stems but not the roots,
and that plants later re-sprout. Regardless, the loss of a sig-
nificant amount of biomass at such a young stage must
severely affect plant fitness.
Anisandrus dispar (F.) girdles and kills branches and
young trees in fruit tree orchards in the USA, where it is
introduced (Hubbard, 1897). It is likely that there are other
ambrosia beetles with similar behavior.
Conophthorus females bore in from the base of a devel-
oping pinecone and girdle it, cutting the conductive tissues
and killing the cone whether or not a brood is successfully
produced (Hedlin et al., 1980; Mattson, 1980). After gir-
dling the cone, they tunnel in a more or less straight line
along the cone axis.
Curiously, unlike with other wood borers, there seem to
be few species, which have been recorded as girdling
branches, twigs, or the stems of seedlings or saplings. Gir-
dling not only disables plant defenses, but it also alters
physical and nutritional qualities of the resource
(Forcella, 1982; Dussourd and Eisner, 1987; Hanks,
1999). Girdling is a widely used strategy in Cerambycidae
(Forcella, 1982; Ferro et al., 2009) and in addition to mit-
igating plant defenses such as sap flow (e.g., Sthenias gri-
sator:Duffy, 1968), girdling may alter favorably the
nutritional quality of the girdled twig by trapping and con-
centrating nutrients normally transported from the leaves
(Forcella, 1982). Interestingly, Forcella (1982) reports that
the cerambycid Oncideres cingulata (Say) cuts phloem
tissues when girdling, but not xylem, so parts distal to the
girdle remain alive. To our knowledge, nobody has inves-
tigated this behavior in bark and ambrosia beetles to
determine if girdling concentrates nutrients, or simply
disarms plant defenses (Dussourd and Eisner, 1987;
Hanks, 1999).
On the surface, it would seem that girdling by ceram-
bycids and scolytines are not analogous, in that ceram-
bycids girdle a branch or twig first and oviposit distal to
the girdle afterwards, while the girdling of scolytines is pri-
marily during egg gallery construction and goes on over
days. Indeed, that scolytines girdle small diameter breeding
material in the course of constructing egg tunnels may
simply be the optimal behavior for spacing of offspring
in the resource medium. Nevertheless, the girdling benefits
mentioned above are substantial, and could select for such
behavior in scolytines: there are species of Carphobius and
Thysanoes that seem to be specialized to breeding in twigs
and branches girdled by cerambycids (S. L. Wood, 1982),
suggesting that scolytines reap the same girdling benefits
as do longhorn beetles. Depending on the temperature
and the size of the beetle with respect to the diameter of
the host material, a tunnel that completely severs phloem
tissues (the first 360-degree turn) might take only a day
or two to complete. It seems clear that girdling is an
adaptive strategy in at least Conophthorus. If girdling is
more than incidental in, for example, twig-breeding species
or species breeding in herbaceous stems or vines, we would
expect to see that spiraling tunnel construction is always
outwards from the initial spot of entry (as described for
Xylocleptes bispinus (F.) in Clematis vines: L€
ovendal,
1898), while it would be random if girdling was not
important.
Herbiphagy is relatively rare in Scolytinae, but many
herbiphagous species do attack live plants (see
Section 3.4). Attacks on stems can kill the plants.
Spermatophagous species (Section 3.6) usually kill the
live seeds in which they breed, and may well have signif-
icant impacts on regeneration of certain host trees
(Janzen, 1971, 1972; Wood, 2007). Palm seed mortality
due to Coccotrypes can be up to 100%, though it varies
much from place to place and year to year (Janzen, 1972;
Kirkendall, unpubl.). Other Coccotrypes species breed in
and often kill live seedlings (the viviparous propagules)
of mangrove trees, affecting mangrove forest communities
(Sousa et al., 2003; see Section 3.4).
3.9.3 Breeding in Live Plant Parts without
Causing much Damage
In exceptional cases, bark and ambrosia beetles breed in
live plants seemingly with little or no damage to the host.
Two unique examples can be found in the large neotropical
genus Scolytodes, both in Costa Rica; both were dis-
covered by the extraordinary young naturalist Kenji
Nishida, who was then doing his Master’s research at
the University of Costa Rica. Scolytodes ageratinae Wood
galls a small, high elevation herbaceous plant, Ageratina
cf. ixiocladon (Asteraceae) (Nishida, pers. commun.);
galled plants seem otherwise healthy, but may have lower
fitness than ungalled. No other galling Scolytinae are
known anywhere in the world. The congener Scolytodes
gunnerae Wood breeds in the leaf petioles of two montane
Gunnera species. The plants, known locally as poor man’s
umbrella (la sombrilla de pobre), have extremely large,
rounded leaves 1–2 m in diameter and sprout in a whorl
from a very short central stem. The beetles breed in
106 Bark Beetles
irregular cave-type galleries in the several-cm-thick, fleshy
petioles of healthy leaves (Figure 3.6). Old tunnels heal
over, and though plant fitness has not been measured,
the large leaves seem unaffected by the presence of a
few small bark beetle galleries, and plants with colonized
leaves seem to flower and fruit normally (Kirkendall,
unpubl.). Again, this feeding mode, i.e., breeding in the
fleshy petioles of large leaves, was totally unexpected
and is unique to S. gunnerae.
In addition, a handful of ambrosia beetles tunnel in the
wood of healthy live trees. Xyleborus vochysiae Kirkendall
is a large inbreeding ambrosia beetle that has only been
observed to colonize standing live Vochysia ferruginea
Mart. (Vochysiaceae) in Costa Rica (Kirkendall, 2006).
About three-quarters of the standing trees in a 7-year-old
plantation were attacked (but multiple felled trees were
not), and almost every tree surveyed in a 20-year-old sec-
ondary forest had the characteristic entry holes of this
species, although it appeared that most attempted coloniza-
tions had failed. The interaction between the beetles and
their host plants was not studied, but there were no signs
of wilting or loss of leaves in the affected trees as might
be the case if they were vectoring an aggressive fungus.
This rare species has only been collected from this one host
species, in contrast to other tropical Xyleborus, which
usually can be found in hosts of several to many different
plant families.
Corthylus columbianus is a common ambrosia beetle
species in hardwood forests of eastern North America
(S. L. Wood, 1982;Majka et al., 2007), where it breeds
in trunks of healthy, vigorous trees. Hosts appear to be unaf-
fected, and old beetle entrance tunnels are gradually
covered over by secondary tree growth. Fungal staining
from old tunnel systems remains in the wood, making pos-
sible the study of historical distributions and population
density fluctuations (Crozier and Giese, 1967b; McManus
and Giese, 1968; Milne and Giese, 1969). Interestingly, a
different Corthylus with similar biology does kill its host
trees. Corthylus zulmae Wood breeds in the trunks of live
native alders (Alnus acuminata Kunth; Betulaceae) in plan-
tations in Colombia (Gil et al., 2004; Jaramillo et al., 2011).
Fungi associated with this species seem to be responsible
for tree death. Their biologies being so similar, the lack
of harm caused by C. columbianus must be due to the
low virulence of its ambrosial fungus.
In most of the examples of Scolytinae or Platypodinae
breeding in live trees there is little damage to the tree itself,
though the value as a timber resource may be reduced.
However, the tunneling of Megaplatypus mutatus (Chapuis)
in the trunks of various hardwoods can weaken the struc-
tural integrity of its hosts to result in stem breakage and
mortality, and it is considered a pest of plantations
(Santoro, 1963; Gime
´nez and Etiennot, 2003; Girardi
et al., 2006; Alfaro et al., 2007; Zanuncio et al., 2010).
4. EVOLUTIONARY ECOLOGY OF
REPRODUCTIVE BEHAVIOR
Bark and ambrosia beetles do not dazzle the eye as do
longhorn and jewel beetles, or please the ear as do crickets
and katydids, but few if any insect groups exhibit such an
intriguing variety of reproductive behavior as do bark and
ambrosia beetles (Kirkendall, 1983, 1993; Kirkendall
et al., 1997; Costa, 2010). In most insects, males leave
females immediately or soon after copulation; in most bark
beetle species, males remain with females in their tunnel
systems until most or all eggs have been laid. Only a few
examples are known where males do not join females in gal-
leries and remain for at least a week or more. Most insects,
and most bark and ambrosia beetles, outbreed, and the
dangers of inbreeding are well documented; nonetheless,
species reproducing by brother/sister mating are wide-
spread and abundant, and have been mating incestuously
for tens of millions of years. Outbreeding taxa vary in
how the two sexes meet (mate location), how long males
stay with females (male residency), and with how many
females individual males are mated simultaneously (mating
systems). Among outbreeders we find male/female pairs
(which in some species mate for life), males with harems,
and numerous instances of bigyny, i.e., species in which
males nearly always mate with exactly two females, a
mating system virtually unheard of outside of Scolytinae.
There are also four forms of parthenogenesis (clonal repro-
duction) in this group: thelytoky, in which females produce
only daughters; pseudogamy (also known as gynogenesis),
in which females mate with males but produce only
daughters, and only the mother’s genes are passed on to off-
spring; arrhenotoky, in which daughters are formed sex-
ually and are diploid, but sons are produced by the
hatching of unfertilized eggs and are haploid; and pseudoar-
rhenotoky, or paternal genome elimination, in which
daughters are formed sexually and are diploid, and males
arise from fertilized eggs but express and pass on only genes
from their mothers.
4.1 Mating Behavior
4.1.1 Fighting
Newly arriving conspecifics are easily repelled by bark and
ambrosia beetles ensconced in tunnel entrances. Physical
combat between members of the same sex takes place pri-
marily early in the colonization phase, usually while a
member of the pioneering sex is beginning to tunnel or
shortly after pairs have formed (Blackman, 1931; Goeden
and Norris, 1965; Fockler and Borden, 1972; Salonen,
1973; Beaver, 1976; Petty, 1977; Vernoff and Rudinsky,
1980; Kirkendall, 1983; Swedenborg et al., 1988, 1989;
Jordal, 2006; Smith and Cognato, 2011). Wandering males
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3107
will also try to enter active gallery systems, but are blocked
from entering by resident males (McGehey, 1968; Oester
and Rudinsky, 1975; Rudinsky and Ryker, 1976; Oester
et al., 1978, 1981). Only rarely do intruding males succeed
in replacing males already in tunnels (Vernoff and
Rudinsky, 1980). Male/male competition is common in
female-initiated mating systems (such as in Tomicus,Den-
droctonus,Pseudohylesinus,orScolytus) but females have
been observed fighting in male-initiated mating systems
(Nord, 1972).
4.1.2 Courtship
Courtship in both Scolytinae and Platypodinae takes place
with both individuals facing forward, so physical interac-
tions during courtship are between the front of the courting
individual and the back end of the courted one. Ancestrally,
males court females, as is the general rule in insects and
other arthropods (and indeed in animals as a whole).
However, females court males in all known cases of harem
polygyny and in some monogynous species as well, such as
in all Platypodinae, monogynous species of Scolytodes, and
the monogynous genera of Corthylini; it has been hypothe-
sized that, for most cases, monogynous species with such
sex role reversal are likely derived from harem polygynous
lineages (Kirkendall, 1983).
Acoustic communication is a key component of inter-
sexual selection during courtship, but may not always
be sufficient by itself for species discrimination (Lewis
and Cane, 1992). It appears that almost all Scolytinae and
Platypodinae stridulate (Barr, 1969; Sasakawa and
Yoshiyasu, 1983; Lyal and King, 1996), though stridulation
has been secondarily lost in some species (Barr, 1969;
Sasakawa and Yoshiyasu, 1983). Stridulation at the
entrance to or inside the gallery system is a key component
of courtship in Scolytinae (Barr, 1969; Swaby and
Rudinsky, 1976; Rudinsky et al., 1978; Rudinsky, 1979;
Rudinsky and Vallo, 1979; Oester et al., 1981; Ryker,
1984; Garraway, 1986; Ytsma, 1988; Swedenborg et al.,
1989; Lewis and Cane, 1992; Ohya and Kinuura, 2001),
and in Platypodinae (Chapman, 1870; Ytsma, 1988; Ohya
and Kinuura, 2001; Kobayashi and Ueda, 2002). Stridu-
lation is also used in male/male and female/female compe-
tition (Rudinsky and Michael, 1974; Rudinsky, 1976;
Swaby and Rudinsky, 1976; Oester and Rudinsky, 1979;
Rudinsky and Vallo, 1979; Oester et al., 1981;
Swedenborg et al., 1988, 1989) and when predators attempt
to enter a gallery system (Roberts, 1960); Wood (2007)
reports that Dendrosinus bourreriae Schwarz adults
working under bark in a branch “buzzed” for several
minutes when the branch was disturbed, sounding like a
nest of bees had been disturbed.
Courtship involves an interaction between acoustic and
chemical communication (Rudinsky et al., 1976; Rudinsky,
1979), and where it has been studied in detail, courtship
behavior also may include bumping (frons to declivity),
antennal tapping or drumming on the declivity, brushing
of antennae or the antennal scape setae against the elytra,
and mandibular gnawing (Blackman and Stage, 1924;
Petty, 1977;Oester et al., 1981; Swedenborg et al., 1988;
Jordal, 2006; Smith and Cognato, 2011). In the platypodine
Doliopygus conradti Strohmeyer, females and males
engage in a “tug-of-war,” where females attempt to pull
males out of newly started tunnels with their mandibles
and males resist; if they ultimately succeed, the female
can then enter the gallery, and mating takes place with
the male on the surface and the tip of the female’s abdomen
protruding from the entrance (Browne, 1962). In a similar
fashion, courting females tug on male Platypus quercivorus
Murayama (Ohya and Kinuura, 2001), so this behavior may
be common in Platypodinae.
Besides the tactile components of bumping, brushing,
stroking, and other rhythmic forms of physical contact
between males and females during courtship, there is likely
an olfactory or “taste” component as well: though little
investigated in bark and ambrosia beetles, interspecific dif-
ferences in cuticular hydrocarbons are important in species
recognition in other insects (Singer, 1998; Howard and
Blomquist, 2005) and such differences have been found
when looked for in bark and ambrosia beetles (Page
et al., 1990a, b, 1997; Sullivan et al., 2012).
Although courtship mostly occurs at or in the entrance
or nuptial chamber, for at least some Scolytinae, mating
can also occur during pre-dispersal feeding in the previous
year’s breeding material, hibernating sites, or feeding
tunnels in branches or twigs (Kirkendall, 1993; McNee
et al., 2000). Although it is likely that courtship patterns,
including which sex courts, are similar to those that occur
around or in gallery systems of the same species, nothing
is known about mating behavior before dispersal and colo-
nization of fresh breeding material.
4.1.3 Copulation
Females of at least outbreeding Scolytinae and Platypo-
dinae copulate more than once, even if with the same indi-
vidual male. Evidence comes from both watching
individuals in nature and observing beetles in semi-natural
conditions such as thick sheets of bark between plates of
glass. Many authors have reported that bark and ambrosia
beetles mate repeatedly during gallery construction
(Gossard, 1913; Blackman and Stage, 1924; Doane and
Gilliland, 1929; Hadorn, 1933; Hansen, 1956; Reid,
1958; Gouger et al., 1975; Petty, 1977; Garraway, 1986).
In some cases, copulation seems to be restricted to the
period when females are still on or near the surface or only
in the early stages of oviposition (Hadorn, 1933; Gouger
et al., 1975; Campobasso et al., 2004).
108 Bark Beetles
Copulations themselves are brief, lasting from
10 seconds to a few minutes at most (Blackman and
Stage, 1924; Hadorn, 1933; Reid, 1958; Gouger et al.,
1975; Garraway, 1986). In the mountain pine beetle
(Dendroctonus ponderosae Hopkins), coupling lasts
10–60 seconds and is repeated about once per day, and less
frequently after egg laying commences (Reid, 1958). For
two species of harem polygynous Ips,Garraway (1986)
reports that copulation takes ca. 10 seconds, and that
females beginning oviposition are mated “frequently.” In
I. avulsus, copulation averages 35 seconds and females
mated three times at 10-minute intervals, after which the
female walled herself off from the nuptial chamber with
tightly packed frass in the egg arm (Gouger et al., 1975).
Platypodinae presumably mate only in the earliest
stages of tunneling; copulation is probably not possible
inside the gallery system, and takes place with the male
on the bark surface and the female in the tunnel entrance.
Courtship and copulation in Platypodinae is described
and illustrated in Jover (1952). There is no nuptial chamber
in the tunnel systems of these ambrosia beetles, and copu-
lation is accomplished by the male exiting the tunnel
entrance and allowing the courting female to enter, then
copulating with the male on the surface and the female in
the tunnel entrance. No deviations from this general pattern
have been reported for Platypodinae.
4.1.4 Repeated Mating: the Key to Evolution of
Prolonged Male Residency?
The fact that females are receptive during part or most of the
egg laying period provides an explanation for the evolution
of mate guarding, and ultimately of male residence.
Lissemore (1997) attributed male residency in Ips pini
(Say) to the need for males to copulate repeatedly with
females in order to fully displace sperm from previous
matings. Many Ips females joining males already have
sperm stored in their spermathecae; in such cases,
Lissemore (1997) found that males require about 5–7 days
of repeated copulations to attain near-complete paternity.
Repeated copulations may function generally as paternity
assurance: half of all T. piniperda females colonizing
breeding material have been inseminated during the pre-
vious year’s maturation feeding in shoots or while overwin-
tering at the bases of trees (Janin and Lieutier, 1988), and in
an Israeli population Mendel (1983) found nearly all
females of Orthotomicus erosus (Wollaston) had been
inseminated after overwintering in dense aggregations.
Much lower levels of pre-colonization insemination are
probably more usual (reviewed by Kirkendall, 1993;
Bleiker et al., 2013), but there is a clear potential for sperm
competition in many Scolytinae, and the evolutionary
response has been repeated copulation. Mating prior to
gallery system construction may, however, be largely
confined to species that are not ambrosia beetles, species
in which aggregations of young adults occur during fall
maturation feeding or in overwintering clusters before
young adults emerge and disperse. The importance of this
distinction will become apparent in our discussion of the
evolution of alloparental care (Section 5.3).
We have discussed repeated copulation from the point
of view of males. From a female point of view, repeated
copulations (continuous sexual receptivity) may be an
adaptation for extending male residency, thus gaining the
benefits of male burrow blocking and frass removal. But
it also may increase the fitness of her offspring by diluting
and eventually replacing sperm from pre-dispersal matings;
this becomes an advantage when some proportion of early
matings are with relatives, and using early sperm then pro-
duces offspring with inbreeding depression.
Thus, males that stay in order to mate repeatedly with
the same female gain offspring through increased paternity
as well as increased female oviposition rates, while females
gain in fecundity (as long as males remove frass) and
produce outbred offspring. It is a short step from males
staying long enough to ensure maximum paternity to the
evolution of paternal care (Section 5.3).
4.2 Mating Systems
Most bark beetles outbreed, as do most insects, but both
regular inbreeding and parthenogenesis (clonal repro-
duction) have evolved in Scolytinae. Outbreeding taxa vary
in how the two sexes meet (mate location), how long males
stay with females (male residency), and with how many
females individual males are mated simultaneously (mating
systems).
Mating system diversity and evolution has been
reviewed by Kirkendall (1983; see also Kirkendall,
1993). Outbreeding bark and ambrosia mating systems
are classified by how many females breed simultaneously
with the same male: one, monogyny; regularly two, bigyny;
several to many, harem polygyny. For consistency,
inbreeding is referred to as inbreeding polygyny, when clas-
sifying mating systems based on numbers of females
(Kirkendall, 1983). In a handful of species, it appears that
both multiple males and multiple females are in contact
and mating is indiscriminate: these systems are referred
to as colonial mating or polygamy.
Another mating system factor is male residency, how
long males remain with females after copulation. Males
do stay with females in most species. The species in which
males do not stay for an appreciable amount of time are scat-
tered among four unrelated tribes (Hylesinini, Diamerini,
Scolytini, and Corthylini (subtribe Pityophthorina)
(Kirkendall, 1983). We will treat male residency in
Section 5, where we discuss it in the contexts of the evo-
lution of subsocial behavior and paternal care. A detailed
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3109
overview of variation in how long males remain in gallery
systems can be found in Kirkendall (1983), and arguments
for the evolution of prolonged male residency are developed
in that review and in Kirkendall (1993), and in Section 5.
Generally, the pioneering sex initiates tunneling in fresh
breeding material, and is located by the following sex; the
second-arriving sex is attracted either to host odors, odors
from boring dust, pheromones, or a combination. Members
of the pioneer sex are also attracted, which often results in
densely colonized host material. In the vast majority of
species, males stay for a week or more, guarding the
entrance and removing frass; commonly, males depart near
or after females have finished ovipositing, and they may
even die in the tunnel system (Kirkendall, 1983).
4.2.1 Monogyny
The ancestral mating system for Scolytinae is almost cer-
tainly female-initiated monogyny, and it is still the predom-
inant mating system in bark and ambrosia beetles
(Kirkendall, 1983;Figure 3.4). Nearly half of all genera
have monogynous species, and nearly all tribes
(Table 3.3), and most of these (especially in more basal lin-
eages) are female initiated.
Male-initiated monogyny is the rule in Platypodinae, but
rare in Scolytinae. In Bothrosternini, it is found at least in
pith-breeding species, in Sternobothrus and certain Cne-
sinus (Beaver, 1973). The sex initiating mating is not
known for most species in the tribe, but it does seem that
all species are monogynous (Kirkendall, 1983). Monog-
ynous species of Scolytodes (a genus with both monogyny
and harem polygyny) are male initiated (Kirkendall, 1983;
Kirkendall, pers. observ., Scolytodes species in Cecropia
petioles). The remaining examples are from the Corthylini,
a tribe with both monogynous and harem polygynous
genera. As far as is known, almost all Corthylini are male
initiated, including the monogynous genera, both those that
are phloeophagous and those that are xylomycetophagous
(Kirkendall, 1983). Exceptions occur in the large phloeo-
phagous genus Pityophthorus, where female initiation
may have re-evolved in a few twig breeders; cone beetles
in the close related genus Conophthorus are also monog-
ynous and female initiated (see next subsection).
As far as is known, without exception, Platypodinae are
monogynous, and males seek out new host material and ini-
tiate tunnel construction (Jover, 1952; Kalshoven, 1960b;
Browne, 1961; Kirkendall, 1983). That almost all Platypo-
dinae are male-initiated monogynous species suggests that,
once evolved, male initiation is evolutionarily stable
(Kirkendall, 1983). Details of mating systems are not
known for Mecopelmus, which is phloeophagous, and Sche-
dlarius, which breeds in fungus-rotted wood of Bursera
(Wood, 1993). Jover (1952) describes the outcome (appar-
ently with several platypodine species) of introducing a
second female to tunnel systems occupied by mated pairs.
These females were accepted by the male, but the second
female soon abandoned the gallery and left. His observa-
tions suggest that monogyny in Platypodinae may be main-
tained by the decisions of secondary females, rather than by
any active resistance by males or primary females, but it
would be informative to see if similar experiments con-
firmed these briefly reported results.
Male-initiated monogyny in Scolytinae tends to occur in
species or genera that otherwise are dominated by harem
polygyny (Kirkendall, 1983). These species breed in
resources where more than one female cannot breed simul-
taneously without dramatic larval mortality due to
intrabrood competition; hence, it is not advantageous for
females to join already-mated males.
4.2.2 Reversions to Female-initiated Mating
Systems
Kirkendall (1983) argued that colonization by males should
be a stable strategy, especially when sex attractant phero-
mones are involved. Females coming to already established
males avoid considerable risks and time investment asso-
ciated with finding usable host material; when they can
enter tunnels immediately, they also reduce their risk of
being consumed by surface-active predators such as
checkered beetles (Cleridae), ants, and foraging birds.
Nonetheless, reversion to female colonization has occurred
in cone beetles (Conophthorus) and in a few twig-breeding
Pityophthorus species, both corthylines. In almost all
Corthylini, males initiate gallery construction. Cone beetles
TABLE 3.3 Number of Scolyinae Genera and Tribes with at Least One Species having the Given Mating System
(247 total genera, 26 total tribes)
Number of Taxa with at Least One Species MG BG HP Col Inbr ?
Genera 118 19 27 3 54 45
Tribes 24 8 8 2 9 17
Some genera and tribes are represented in more than one category. MG ¼monogyny; BG ¼bigyny; HP¼harem polygyny; Col ¼colonial polygyny
(polygamy); Inbr ¼inbreeding; “?” ¼mating system unknown. Data from Appendix.
110 Bark Beetles
are a monophyletic corthyline group similar to
Pityophthorus genetically, morphologically, and in pher-
omone components (pityol, conophthorin) (S. L. Wood,
1982;Dallara et al., 2000; Rappaport et al., 2000;
Cognato et al., 2005;Conophthorus biology is also dis-
cussed in Section 3.6). An example from Pityophthorus is
P. pubescens (Marsham). Most Pityophthorus are harem
polygynous phloeophages in branches or trunks of hard-
woods and conifers, and are distributed around the world;
males initiate gallery systems, and where known, produce
attractant pheromones. Pityophthorus pubescens is one of
several twig breeders that have reverted to monogyny,
and in this species females initiate gallery construction
and also produce a sex pheromone (Lo
´pez et al., 2013).
What these species seem to have in common is that
females spread their oviposition among many host resource
units, rather than putting a large number of eggs in one
resource over a long period of time as is the case in most
bark and ambrosia beetles. Perhaps the short female resi-
dency time reduces advantages to males of staying with
females, which in turn leads to females needing to initiate
at least subsequent galleries alone. Once that behavior is
in place, it is possible for female initiation of the first egg
tunnel to evolve, though it is not clear what balance of
selective forces would lead to its evolution.
Females also colonize in parthenogenetic (thelytykous)
species (Pityophthorus puberulus (LeConte): Deyrup and
Kirkendall, 1983) and of course in inbreeders (since males
do not disperse), including lineages likely derived from out-
breeders with male initiation such as the Araptus laevigatus
Wood complex. In Pityophthorus and Araptus, this may
have evolved either after female initiation re-evolved, or
directly from male initiation (which predominates in these
genera and their allies).
4.2.3 Bigyny
Regular bigyny has evolved repeatedly in Scolytinae,
from both harem polygynous and monogynous ancestors.
Systems in which males regularly have two females
are found in 19 different genera, in eight tribes; seven
genera are from the Micracidini, in which most genera
are bigynous. Several otherwise monogynous genera
have one or a few species that are bigynous. In the
Phloeosinini, bigynous species are found in two oth-
erwise monogynous and (mainly) phloeophagous
genera, Phloeosinus and Chramesus.Chramesus has the
bigynous species C. incomptus Wood, which makes
biramous diagonal galleries in Clematis shrub stems
(S. L. Wood, 1982).
We can find no references to regular, simultaneous
bigyny in other animals. In fish and birds, at least, occa-
sional bigyny in monogynous species seems to occur when
male territories are of sufficient size and quality to overlap
territories of two females. In such cases, most males are
monogynous, and a few (in fish, usually larger males) are
bigynous. That regular bigyny is only known from Scoly-
tinae must, then, be related to geometric constraints on
egg tunnel construction (situations that force tunnels to
diverge at 180). But this does not explain why the vast
majority of bark beetles with transverse or longitudinal
biramous tunnel systems (i.e., systems in which the two
tunnels do diverge at or nearly at 180) remain monogynous
or are only occasionally, not regularly, bigynous.
That bigynous species rarely have more than two
females is easier to understand. When egg tunnels are con-
strained to run either parallel to the wood grain or perpen-
dicular to it, adding the work of a new female means adding
a tunnel parallel to, and close by, the tunnel of another ovi-
positing female, which should result in extremely high
larval mortality in species where larvae must tunnel long
distances to acquire enough resources (Kirkendall, 1984;
Løyning and Kirkendall, 1999). In most such situations,
females should be selected to avoid joining bygynous
systems.
By the same reasoning, for species where egg tunnels
are all longitudinal or all transverse, polygyny is only pos-
sible where resource quality is high and larval tunnels cor-
respondingly short; in such cases, most males have four
(maximum of two parallel arms running in one direction)
or less females. In cases where females join males with four
females, the joining female(s) will suffer large losses of off-
spring due to competition (Schlyter and Zhang, 1996; Latty
et al., 2009; Kirkendall, 1989). This constraint on harem
size is weak or nonexistent in harem polygynous species
producing star-shaped gallery systems with long egg
tunnels, however; egg tunnels diverge more and more, as
they progress, steadily reducing intraharem competition
for resources. Star-shaped systems are especially common
in genera such as Pityophthorus,Scolytodes,Pityogenes,
Pityokteines, and Polygraphus.
4.2.4 Harem Polygyny
Simultaneous polygyny (harem polygyny and bigyny) has
evolved only sporadically in more basal taxa (Figure 3.7;
reviewed in detail in Kirkendall, 1983). Altogether, 39
genera in 11 tribes have species that are harem polygynous
or bigynous (Appendix). Based on Figure 3.7, it appears
that polygyny has evolved at least 12 times in Scolytinae;
the number of independent origins is certainly higher, given
that there are multiple occurrences of polygyny in each of
the predominantly monogynous genera Scolytus and
Phloeosinus, and at least some of the polygynous species
are not related to other polygynous species in the same
genus. Harem polygyny is found in 26 genera in eight tribes.
It is the predominant mating system in Ipini, and common in
Corthylini and Polygraphini.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3111
Harem polygyny is relatively rare in animals. In bark
and ambrosia beetles, polygyny takes the form of resource
defense polygyny, where males accrue multiple mates
because they control critical breeding resources capable
of supporting the reproduction of more than one female
(Emlen and Oring, 1977; see also Searcy and Yasukawa,
1989). The key question in polygynous mating systems is
why females join already mated males, if unmated males
are available. Females joining a mated male rather than
an unmated (or less mated) one may suffer decreased
fecundity in more crowded systems and decreased offspring
survivorship due to within-harem competition (Kirkendall,
1989). This must be outweighed by the costs in time,
energy, and predation risk of searching for an unmated
(or less mated) male. If mated males control sufficiently
high quality breeding resources, the positive effects of
resource quality on fitness can outweigh the costs of joining
a mated male. This resource-based argument for the evo-
lution of simultaneous polygyny is encapsulated in the
polygyny threshold model, which though developed and
tested in the context of bird mating systems, would seem
to apply well to bark and ambrosia beetles (Kirkendall,
Regular inbreeding (biased offspring sex ratio
Polygynous breeding, with two or more females
Normal outbreeding, monogynous
*
*
*
*
**
*
*
*
*
FIGURE 3.7 Phylogenetic tree of Scolytinae with mating systems indicated (see inset legend). Harem polygyny includes bygyny. Stars indicate
genera or lineages in which the mating system is rare (one or just a few species).
112 Bark Beetles
1983). Kirkendall (1983) postulates that the harem
polygyny threshold model is most likely to lead to the evo-
lution of polygyny in these beetles when resource quality is
highly variable (not uniformly high or low). Variable
resource quality leads to some males being in high quality
resource patches capable of supporting high fecundity of
several females, while other males sit in low quality patches
and will be largely ignored by searching females. See
Kirkendall (1983) for a more detailed development of the
argument and for data supporting it.
For species where egg tunnels are all longitudinal or all
transverse and hence run parallel to each other if on the
same side of the gallery system, polygyny is only possible
where resource quality is sufficiently high and larval
tunnels correspondingly short. Support for this hypothesis
comes from observations that males in fact refuse entry
to additional females after having acquired their normal
complement (Borden, 1967; Swaby and Rudinsky, 1976),
and that once having achieved large harems, males of
several species have been shown to be less attractive or
to reduce pheromone emission (Kirkendall et al., 1997).
Kirkendall (1983) suggests that females in large harems
do not suffer a fitness cost to joining harems. Available data
also suggest that in harems with only three of four females,
it is possible for females to avoid within-harem competition
if they space their egg galleries optimally, even in systems
where egg tunnels run parallel to each other as they do in
Ips (Kirkendall, 1989; Schlyter and Zhang, 1996; Latty
et al., 2009).
In the extreme case of no available solo-male territories,
the only option for females is to join mated males (i.e.,
harems). Mortality of the initiating sex is thought to be quite
high in bark and ambrosia beetles, due to the difficulties of
locating breeding material before exhausting energy
resources, mortality from above-bark predation, and deaths
due to residual or active host tree defenses. If males are the
pioneer sex, and if mortality is high enough, then one would
expect considerable pressure from late-arriving females on
blocking males to allow them entry, even when one female
is already in the gallery system. Polygyny can then evolve
as long as the net change to male fitness is positive and the
fitness of joining females greater than zero, and assuming
that the first-arriving females cannot prevent entry of
further females. Put more simply, polygyny can evolve if
it pays males to allow more than one female to enter, and
if females joining mated males can successfully produce
offspring. Note, however, that in current harem polygynous
species, unmated males are relatively frequent (review and
original data in Kirkendall, 1983; Schlyter and Zhang,
1996; Latty et al., 2009).
4.2.5 Colonial Polygyny
We have categorized three genera in two tribes as having
species with colonial polygyny (Table 3.3): Aphanarthrum
and Crypturgus (Crypturgini), and Cyrtogenius (Dryo-
coetini). None of the species we call colonial have been
studied in detail, but they appear to have multiple males
and multiple females in the tunnel systems. It is possible
that some of these instances are of multiple male/female
pairs sharing a system of tunnels, but it seems more likely
that no pair bonds are formed and both sexes mate with
several individuals of the opposite sex. It must be difficult
for males to maintain exclusive access to females in a
many-branched tunnel system. In the phloeophagous Cyrto-
genius brevior (Eggers) in Fiji, gallery systems are
described as having many branches, with several adults in
each branch; Roberts (1976) collected 20 males and 32
females from 11 or 12 galleries. Other species in the genus
are monogynous, and phloeophagous or xylophagous
(Browne, 1961, 1963; Roberts, 1976). Similarly, all Cryp-
turgus species are found in networks of interconnected
tunnels with many females and males in the same colony
(Blackman and Stage, 1918; Chararas, 1962). Jordal
(2006) reported on systems of interconnected tunnels with
multiple individuals in Aphanarthrum species breeding in
succulent Euphorbia species and suggested that promis-
cuous systems such as these evolve in lineages of inquilines,
i.e., species that regularly use tunnels of other species as a
starting point for their own egg galleries. This behavior is
the norm, for Crypturgus species, and has also been
observed in Aphanarthrum (Jordal, 2006).
4.2.6 Inbreeding Polygyny
Inbreeding polygyny is not unique to Scolytinae; regular
brother/sister mating is found in a wide range of organisms,
ranging from eyelash mites to naked mole rats, but it has
evolved especially often in bark beetles. Extreme
inbreeding has evolved eight times in Scolytinae, and is
represented in nine different tribes (Table 3.3). About
27% of all described Scolytinae are thought to breed regu-
larly by brother/sister mating. Of all inbreeding species,
97% come from two major species radiations. The largest
inbreeding clade is that of 1336 species from 37 genera
of Xyleborini plus three genera of inbreeding Dryocoetini,
22% of all Scolytinae (Tables 3.3 and 3.4,Appendix). This
clade has been inbreeding regularly for about 20 million
years (Jordal and Cognato, 2012). The second largest clade,
the inbreeding Cryphalini, comprises 238 species divided
among six genera. Its age is estimated to be ca. 50 million
years (Jordal and Cognato, 2012). Despite the evolutionary
success of the two major clades and ecological success
of many inbreeding species, there is no evidence that
inbreeding leads to diversification (Jordal and
Cognato, 2012).
While many inbreeding clades are ambrosia beetles,
there is no evidence that ambrosia feeding in itself predis-
poses a lineage to evolving inbreeding. Inbreeding has not
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3113
evolved in Platypodinae, Corthylina (the ambrosia beetle
subtribe of Corthylini), or Camptocerus. In six lineages
in which ambrosia feeding and inbreeding co-occur, fungus
farming preceded inbreeding in only three (Jordal and
Cognato, 2012). Actually, the highest transition rates to
xylomycetophagy are from lineages with regular inbreeding
(Jordal and Cognato, 2012).
What is striking from Table 3.4 is that inbreeders mainly
have feeding modes other than the predominant one of
phloeophagy. Kirkendall (1993) analyzed the association
between inbreeding and larva feeding modes for the bark
and ambrosia beetles of North and Central America and
for those of Thailand, Malaysia, and Indonesia. For both
regions, inbreeders are most commonly ambrosia beetles.
For North and Central America, 93% breed either as
ambrosia beetles or in pith, seeds, and fruits, or “diverse“
tissues. In the Southeast Asia fauna, too, those that are
not ambrosia beetles are mainly myelophagous and sperma-
tophagous. Conversely, inbreeding has never evolved in
purely herbiphagous lineages (Kirkendall, 1993), though
a few inbreeders have evolved herbiphagy and some gener-
alists (both ambrosia beetles and phloeophages) are able to
breed in herbaceous tissues. Both Xylosandrus, which breed
in orchids (Dole et al., 2010), and Hypothenemus, which
breed in fleshy tissues, are tissue generalists, with the
exception of H. pubescens, which may breed exclusively
in grass stems (Atkinson and Peck, 1994). Coccotrypes,
which attack mangrove propagules, are also herbiphagous
(Sections 3.4 and 3.9). These examples all come from
inbreeding clades.
The few phloeophagous inbreeders are atypical for
species breeding in inner bark: both Ozopemon and
Dendroctonus breed in large chambers with larvae feeding
communally, as do phloeophagous Hypothenemus and Coc-
cotrypes (Kirkendall, 1993). Communal larval feeding is a
common theme in inbreeders, and one of the most important
factors in the evolution of regular inbreeding. Communal
feeding is associated with all inbreeding lineages whether
they are ambrosia beetles, pith breeders, seed breeders, or
phloem feeders (Kirkendall, 1993; Jordal and Cognato,
2012). In seeds, if colonized only once, a single family
develops in close contact within the confines of a single
seed. In pith, the larvae feed in close proximity in one long
cylinder.
As argued by Kirkendall (1983, 1993), the first step in
the evolution of inbreeding must be pre-dispersal mating.
However, for pre-dispersal mating to be incestuous, young
adults must have developed in close proximity. In most bark
beetle systems, larvae tunnel away from the maternal egg
gallery, and most bark beetles breed in relatively dense
aggregations: any mating before dispersing will usually
be between offspring of different broods. Inbreeding can
only evolve in an outbreeding species if young adults are
in close contact with each other when they mature, as will
happen if they develop together in a common nest as larvae
of one family.
Inbreeding is characterized by two major ecological
patterns (Kirkendall, 1993; Jordal et al., 2001). There is
a latitudinal gradient in close inbreeding: the proportion
of inbreeders in the Scolytinae fauna increases from just
a few species in the far north or far south to being roughly
half of the fauna of lowland tropics. It is likely that there is
also a corresponding elevational gradient (inbreeding
decreases with increasing altitude), though this has not
TABLE 3.4 Occurrences of Inbreeding in Scolytinae (after Kirkendall, 1993; see also Phylogeny in Jordal and
Cognato, 2012)
Lineage Tribe Inbr. spp. Biology
Bothrosternus Bothrosternini 11 Ambrosia beetles
Araptus laevigatus complex Corthylini 9 Seeds, pods, leafstalks, fruits
Cryptocarenus,Hypothenemus,Margadillius,
Periocryphalus,Ptilopodius,Trischidias
Cryphalini 238 Highly variable, but few strictly
phloeophagous (see text); one ambrosia
beetle
Coccotrypes,Ozopemon,Dryocoetiops
+ Xyleborini
Dryocoetini
Xyleborini
168
1168
Seeds, fruits; many highly polyphagous;
Ozopemon is phloeophagous.
Ambrosia beetles
Dendroctonus micans,D. punctatus Hylurgini 2 Phloeophagous
Sueus Hyorrhynchini 5 Ambrosia beetles
Premnobius,Premnophilus Ipini 25 Ambrosia beetles
Xyloterinus Xyloterini 1 Ambrosia beetles
114 Bark Beetles
been thoroughly investigated (but see Kirkendall, 1993).
Inbreeding is also disproportionately common on small
islands, not because outbreeders evolve incestuous mating,
but because inbreeders are more successful colonizers
(Kirkendall, 1993; Jordal et al., 2001). The species–area
relationship differs for the two mating behaviors: numbers
of outbreeding species decrease more rapidly with area
than do numbers of inbreeding species. Jordal et al.
(2001) showed that this pattern was not due to differences
between outbreeders and inbreeders in resource utilization
(feeding modes) or by sampling biases (undercollecting).
Rather, outbreeders are poor colonizers because they
are constrained by Allee effects, density-dependent be-
havioral and ecological factors disproportionately
impacting small populations (Gascoigne et al., 2009;
Kramer et al., 2009). Jordal et al. (2006) postulate that out-
breeders have difficulties successfully establishing new
populations because they are more vulnerable to random
extinctions of small populations, suffer inbreeding
depression, and have difficulties finding mates. Inbreeders,
by virtue of investing minimally in males, and by not
expending time and energy on mate location, have higher
intrinsic rates of increase, and thus are exposed to the
dangers of stochastic extinctions for a shorter period than
are outbreeders.
Repeated inbreeding rapidly produces homozygotic
genomes, which are then passed on intact from one gener-
ation to the next. Regular inbreeding, then, can be con-
sidered to be quasiclonal reproduction, “quasi-” because
outbreeding is always a possibility in inbeeding lineages,
while in most cases truly clonal, parthenogenetic organisms
cannot suddenly shuffle their genes in a bout of sexual
reproduction. Reproduction by extreme inbreeders (species
for which interfamilial inbreeding is the norm), then, is
“clonal” as long as inbreeding continues, but is “reset”
for females mating with unrelated males who manage to
get into a foreign gallery system. Outbreeding individuals
then produce a genetically variable brood with a burst of
heterozygosity.
How often does outbreeding occur in inbreeding lin-
eages, and how does it happen? This is a key question for
understanding why inbreeding has been so successful in
these beetles. Population structure has been investigated
recently for the seed borers Coccotrypes dactyliperda (F.)
(Gottlieb et al., 2009; Holzman et al., 2009) and H. hampei
(Benavides et al., 2005); all found low rates of genetic var-
iation, and large genetic differences between populations,
patterns consistent with high rates of inbreeding. Experi-
ments with X. germanus (Peer and Taborsky, 2005) found
outbreeding depression but no inbreeding depression, as
expected for regular inbreeders. Gottlieb et al. (2009) esti-
mated inbreeding rates and found that they vary highly
between populations but generally reflect high amounts
of inbreeding.
Extreme inbreeders, then, potentially reap the benefits
of clonal reproduction, i.e., replication of successful
genomes from one generation to the next, preserving com-
binations of genes that work well together and conserving
local adaptation. All inbreeders that have been studied in
any detail have evolved adaptive, strongly female-biased
sex ratios, further increasing advantages to inbreeding; out-
breeders invest half their resources in males, while
inbreeders invest minimally. However, this nearly two-fold
advantage in reproductive rate would be largely mitigated if
males significantly increase the reproductive output of their
partners. For this reason, the fitness effects of male resi-
dency are particularly relevant, in understanding the factors
favoring or disfavoring the evolution of regular inbreeding.
It should also be more difficult for inbreeding to evolve in
species where male presence significantly increases female
fecundity or the survivorship of the male’s offspring (see
Section 5.3). There should then be strong selection on
females to bind males to them, which they do by being con-
tinuously receptive, even if females have mated previously
and have sufficient sperm to fertilize all their eggs. Females
breeding alone (and hence using only sperm from a pre-
dispersal mating) would have low reproductive success rel-
ative to outbreeding females.
4.2.7 Partial Inbreeding
As far as can be determined from the literature on
inbreeding Solytinae, almost all instances are examples of
extreme inbreeding, and reproduce regularly by brother/
sister mating (Kirkendall, 1993). The likely exception is
the Palearctic D. micans and its Nearctic sister species D.
punctatus LeConte. These two species may be the best
examples of scolytine species with populations that regu-
larly experience intermediate levels of inbreeding (but
see Holzman et al., 2009). All other inbreeding lineages
in Scolytinae exhibit most characteristics of what
Hamilton (1967) termed a biofacies of extreme inbreeding,
but this Dendroctonus clade does not; their males are only
statistically shorter and lighter in weight than females, and
can fly (Kirkendall, 1993; Meurisse et al., 2008). Further,
D. micans seem to produce more than minimum numbers
of males per brood; typical families have 10–30 males
(Kirkendall, 1993). Dendroctonus punctuatus have simi-
larly large broods with multiple males, and have an average
of about five females per male (N¼37 broods: M. Furniss,
pers. commun.). Other inbreeding scolytines normally
produce broods with just one or very few males, sufficient
to fertilize all their sisters (Kirkendall, 1993). However, as
with all other inbreeding scolytines, mating in D. micans
and D. punctatus occurs before females disperse, and males
do not participate in gallery construction. Inbreeding as
a breeding strategy has not been studied in D. micans or
D. punctatus, but the only genetic study (using protein
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3115
electrophoresis) supports a hypothesis of intermediate
levels of inbreeding, with modest but reduced levels of het-
erozygosity found in both species (Kegley et al., 1997).
That D. micans and D. punctatus do not seem to be fully
committed to inbreeding could have arisen in two ways.
First, it is possible that they are under strong selection to
inbreed and do so most of the time, but that inbreeding
has evolved too recently for males to fully adapt. In this
case, the relatively high numbers of males might be mal-
adaptive, but females might have poor control over the
sex of their eggs. Alternatively, these two species may
indeed be balancing inbreeding and outbreeding, and the
numbers of males produced may be optimal for the levels
of outbreeding occurring in natural populations as well as
for regular partial brood mortality due to Rhizophagus
grandis Gyllenhal predation (discussed in Kirkendall,
1993). We lean towards the latter hypothesis. Inbreeding
must have evolved before D. micans and D. punctatus split.
This split may have been as recent as the Wisconsin glaci-
ation 85,000–11,000 years ago, as argued by Furniss
(1996), but as he pointed out, they differ in 10 discrete mor-
phological characters, and they also differ in karyotype
(Zu
´n
˜iga et al., 2002a, b). Whether or not this level of
differentiation can occur in such a relatively short time is
an interesting question.
Broods regularly merge in epidemic outbreaks of
D. micans, and under endemic conditions, males are fully
capable of wandering from one brood gallery to another,
or even flying to another colonized tree (Meurisse et al.,
2008). Whether or not interfamily matings represent genetic
outbreeding is not known. When there are multiple broods
on a single tree, these may often stem from related females
(Gre
´goire, 1988).
4.2.8 Parthenogenetic Reproduction
Four forms of parthenogenetic reproduction have evolved
in Scolytinae. In thelytoky and pseudogamy, females are
produced clonally and are genetic copies of their mothers.
In the former, no males are involved and populations consist
solely of females, while in the latter, fertilization is required
(by males of the same or a related species) but male
genomes are not used to build the phenotype and are not
passed along to offspring. In arrhenotoky and pseudo-
arrhenotoky, daughters are sexually produced, but males
express and pass on only genes from their mother. Males
are thus functionally haploid in both, though in pseudo-
arrhenotoky, fertilization takes place but then the paternal
genome is eliminated. Since male genomes are produced
by meiosis, males are not clonal.
Obligate or facultative thelytoky is relatively frequent in
weevils, and occurs at least sporadically in over 80 families
of Hexapoda (Normark and Kirkendall, 2009); it has arisen
at least once in Scolytinae, in Corthylini, though there are
several lineages in which it may also occur. Deyrup and
Kirkendall (1983) examined over 500 Pityophthorus pub-
erulus (LeConte) individuals collected from Indiana,
Michigan, and Maine; P. puberulus is the most common
scolytine in dead twigs of native and exotic pines. All were
female, and none contained sperm, not even those taken
from galleries with eggs and larvae. In no case were two
parent adults found in a gallery system. In taxonomic treat-
ments of the genus, Bright (1981) and S. L. Wood (1982)
describe P. puberulus males simply as being identical to
females; but as found by Deyrup and Kirkendall (1983),
Bright (1981) reports that galleries contain only one indi-
vidual. Thus, while it is possible that one or more sexual
populations exist in this widespread species, no confirmed
males are known, and P. puberulus should be considered
parthenogenetic. There have been no subsequent investiga-
tions into this interesting case of thelytoky.
A possible second instance of all-female lineages comes
from S. rugulosus. Gurevitz (1975) reported breeding
repeated all-female generations in the laboratory, from
beetles collected in Israel. Scolytus rugulosus has been
occasionally studied as a pest of fruit trees in its native
Eurasia and as an invasive species in North America, but
no deviations from 1:1 sex ratios have been reported by
other authors, and it seems to be a normally reproducing
monogynous bark beetle everywhere else other than the
Middle East (Gossard, 1913; Kemner, 1916; Chodjaı
¨,
1963; Kirkendall, unpubl.). Parthenogenesis in S. rugulosus
needs to be confirmed.
Finally, there are several groups (Bothrosternus
foveatus Wood and Bright; Dryocoetiops) that have been
treated as inbreeding (Kirkendall, 1993) but where males
have still not been found; in both, close relatives are
inbreeders. Given that males of inbreeders are often tiny
and are rarely collected, it is possible that these groups
inbreed.
In pseudogamy, a form of sperm-dependent partheno-
genesis, eggs must be fertilized to develop, but sperm do
not contribute genetically to the offspring and inheritance
is strictly mother to daughter (Beukeboom and
Vrijenhoek, 1998; Schlupp, 2005). It is a rare reproductive
system, occurring among hexapods in just a few other
orders; in beetles, it is found in a spider beetle (Ptinidae).
Pseudogamy as a reproductive system has evolved at least
twice in Scolytinae, in North American spruce-breeding
Ips, and in a Eurasian pine-breeding Ips (Lanier and
Kirkendall, 1986).
In North America, pseudogamy occurs in the tridens
complex of spruce-breeding Ips (Hopping, 1964; Lanier
and Oliver, 1966; Lanier and Kirkendall, 1986). Three types
of individuals, pseudogamous females, sexual females, and
males, are found in Ips borealis Swaine, I. tridens (Man-
nerheim), I. pilifrons Swaine, and I. perturbatus (Eichhoff).
In all four “species,” pseudogamous females are triploid
116 Bark Beetles
(Lanier and Kirkendall, 1986). As is usually the case
(Schlupp, 2005), pseudogamy has probably originated via
interspecific hybridization. These pseudogamous lineages
form a monophyletic clade (Cognato and Sperling, 2000),
so the phenomenon may have evolved only once in this
species group. For the most part, only the taxonomy
and systematics of these pseudogamous populations have
been studied; virtually nothing is known of the nature of
pseudogamy in these lineages. It seems likely that predom-
inantly or entirely sexual populations were studied in the
ecological investigations of I. perturbatus, which in these
papers seems to have typical Ips biology and equal sex
ratios (Gobeil, 1936; Robertson, 2000).
Interspecific hybridization is much less likely the origin
in I. acuminatus, the Eurasian example of pseudogamy,
though here, too, the parthenogenetic females are triploid
(Lanier and Kirkendall, 1986). Though this pine breeder
occurs from Western Europe to eastern Siberia, China,
and Japan, its reproductive behavior and population
dynamics have only been studied in Europe (Bakke,
1968b; Kirkendall, 1989, 1990; Kirkendall and Stenseth,
1990; Løyning and Kirkendall, 1996; Løyning, 2000;
Meirmans et al., 2006).
Arrhenotoky has arisen once in Scolytinae, producing the
remarkably successful haplodiploid clade comprising Xyle-
borini (nearly 1200 species in 37 genera) and three
inbreeding genera previously placed in Dryocoetini, Cocco-
trypes (129 spp.), Ozopemon (21 spp.), and Dryocoetiops (18
spp.) (Jordal et al., 2002; Cognato et al., 2011; Jordal and
Cognato, 2012). It is well known that bees, wasps, and ants
are haplodiploid, but this system is also found in the one
species of Micromalthidae, many thrips, a few whiteflies
and scale insects, most rotifers, most mites, and some nem-
atodes. The entire scolytine clade is considered haplodiploid,
but this is based on the observations of just a few species of
Coccotrypes and Xylosandrus (Kirkendall, 1993). However,
there are no data that falsify the hypothesis that the entire
clade is haplodiploid, and finding all-male broods in many
species supports the hypothesis (these represent reproduction
by unfertilized females).
Pseudo-arrhenotoky is known from one inbreeding
lineage, Hypothenemus, having been demonstrated in
H. hampei (Brun et al., 1995a, b; Borsa and Kjellberg,
1996a, b;Chapter 11). The phenomenon was discovered ser-
endipitously while studying the evolution of resistance to
insecticides, when it was observed that males always had
the resistance phenotype of their mother, regardless of the
father’s phenotype. Worldwide, there are 181 described
species in the genus (Chapter 11), but only H. hampei has
been studied in this context. It is believed that the entire
genus inbreeds, since in all cases where broods have been
examined, males are rare, and all males known are reduced
in size and flightless, which are characteristics of regular
inbreeders. Further, the most closely related genera also
inbreed. Pseudo-arrhenotoky is a rare breeding system, but
is known in some mites and in mealy bugs (Coccidae). Var-
iation in reproductive systems among closely related
coccids, though, raises a red flag, and the hypothesis that
pseudo-arrhenotoky is characteristic of all inbreeding
Hypothenemus its relatives should be verified.
4.3 Gallery System Form
The general hiking and camping public, including most
entomologists, rarely encounter the insects themselves,
but may well be aware of the consequences of their activ-
ities: dead and dying trees during bark beetle outbreaks,
and the striking engravings seen in older dead wood. Forest
entomologists have long classified these etchings based on
their general form (Barbey, 1901; Swaine, 1918; Blackman,
1922; Chamberlin, 1939), and they are still used today.
Generally, one can deduce the mating system of a
species (especially those breeding in inner bark) from the
form of the tunnel system: single egg tunnels result from
monogyny, a variable number of egg tunnels per system
from polygyny (Figure 3.6). However, when there are
two tunnels, this may result either from a single female
working in two directions or, in a few lineages, from
bigyny. Variously shaped large chambers lacking defined
egg tunnels—cave-type systems—are formed by monog-
ynous species.
Females of phloeophagous Scolytinae disperse eggs in a
wide variety of ways. Most commonly, all eggs laid by a
single female during a given bout of reproduction are
deposited in a single long gallery or in two long galleries
bored in opposite directions. In a few genera, a single
female makes several short tunnels leading away from a
central nuptial chamber; an especially interesting example
is Ips latidens (LeConte), a monogynous species in an oth-
erwise uniformly harem polygynous genus (Reid, 1999).
Most Cryphalini, and a few genera or species from other
lineages, make elongate to roundish chambers, where the
eggs are either spaced around the periphery in egg niches
(as in Procryphalus mucronatus (LeConte), Dacryostactus
kolbei Schauffuss, or Styracoptinus murex (Blandford)),
deposited in egg pockets (Cryphalus kurilensis Krivo-
lutskava, C. exiguus Blandford), or simply laid in clusters
loose in the gallery (Cryptocarenus, some Cryphalus, many
Hypothenemus,Trypophloeus populi Hopkins). Some spe-
cialists, such as Blackman (1922),Browne (1961), and
S. L. Wood, (1982), have thought that cave-type galleries
were “primitive” in bark beetles, but this seems unlikely
given that basal taxa in current phylogenies all make long
egg tunnels.
Ambrosia beetle tunnel systems also show variation in
egg deposition strategies (Browne, 1961). Again, in most
groups, each female constructs a single tunnel or a few long
branches. Tunnels constructed in smaller branches may
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3117
completely encircle the branch, and in very small-diameter
breeding material tunnel systems usually spiral. Eggs are
placed in niches constructed by the mother beetle in Camp-
tocerus, Corthylini, and Xyloterini, reflecting their deri-
vation from phloeophagous ancestors with egg niches;
they are laid in batches loose in tunnels or lenticular
chambers in Xyleborini, as they are in other members of this
clade (spermatophagous or phloeophagous Coccotrypes,
Ozopemon, and relatives), suggesting that the ancestors of
this large inbreeding clade lost the practice of placing eggs
singly in niches. Interestingly, Platypodinae lays eggs in
clusters and larvae feed in the tunnel system, but the last
instar larvae form cradles in which they pupate singly.
Long tunnels give females options for optimally dis-
persing offspring in space, both with respect to resource
quality, resource quantity, host plant defenses, and
intrabrood competition. At the same time, females them-
selves must feed continuously in order to produce large,
protein-rich eggs. In Scolytinae, eggs are generally one-
quarter to one-third or more their mother’s body length
(Kirkendall, unpublished data), while plant tissues they
consume are critically low in nitrogen (White, 1993;
Kirkendall, 1983; Haack and Slansky, 1987; Ayres et al.,
2000). Tunneling, then, fulfills both needs: spacing of eggs
and acquiring nutrients for oviposition. Spatial orientation
of tunnels, placement of eggs in the tunnels, and spacing
of eggs all are highly variable in Scolytinae and almost cer-
tainly are adaptations, but there has been little research in
this area.
4.3.1 Spatial Orientation
Broadly considered, phloeophagous tunnel systems are
classified by the number of egg tunnels (arms) in a system
and by the orientation of the tunnels. Most monogynous
systems can have one (uniramous), two (biramous), or
(exceptionally) more egg tunnels (polyramous). These
tunnels can run with the wood grain (longitudinal or ver-
tical), or perpendicular to the grain of the wood (transverse
or horizontal); biramous systems can also be V-shaped.
Tunnels of some Dendroctonus are long and very irregular
in shape. Chaetophloeus species make single nearly circular
egg tunnels; Pseudips construct C- or S-shaped systems
(uni- or biramous). Polygynous systems are also classified
by egg tunnel orientation, although less often so than are
monogynous systems. In many polygynous taxa, egg
tunnels are clearly oriented either longitudinally (e.g., most
Ips) or transversely (Pityokteines), but others are simply
fairly evenly spaced from each other and form star-shaped
patterns (Polygraphus, most Pityophthorus). Gallery
systems of regularly bigynous species usually are biramous,
with each arm being the work of one female, and these run
directly opposite one another, either longitudinally or trans-
versely, though some species make V-shaped systems (one
female in each arm). Females of Pseudothyanoes each
make both arms of a “V,” the system as a whole resembling
an “X” or “H.”
The adaptive significance of variation in egg tunnel ori-
entation has not been rigorously analyzed, though
hypotheses have been proposed (see Kirkendall, 1983). It
is clear that there are associations with host plants: bark
beetles in oaks (Quercus) and firs (Abies) tunnel horizon-
tally, for example, even though congeners tunnel vertically
in other hosts (Kirkendall, unpubl.). Since newly hatched
larvae tunnel at least initially perpendicularly to the egg
tunnel, the best orientation of the egg tunnel may be deter-
mined by factors selecting for larval tunneling direction: if
it is optimal for larvae to tunnel with the grain of the wood,
for example, then the egg tunnel should be transverse.
Selection on adult or larval tunneling direction can result
from host–plant defenses and physical characteristics of
the host. If the inner bark is too thin to completely contain
larvae as they feed, or if there are other reasons for larvae to
tunnel deeper such that they begin to feed partly in
sapwood, then the more fibrous nature of sapwood becomes
a significant factor, as pointed out by Tra
¨ga
˚rdh (1930).
Tra
¨ga
˚rdh (1930) also found that larval mines when
engraved into the sapwood run strictly longitudinally and
parallel to each other, but if the larval mines are purely in
the inner bark, the mines can wander and can be transverse
to one another. Both oaks and the woody leafstalks of
Cecropia are quite fibrous, and especially small larvae
probably cannot tunnel transversely; tunnels of bark beetles
in oaks, and the smaller species in the cortex of Cecropia
petioles, are transverse, and larvae feed perpendicularly
to the gallery arms (with the wood fibers rather than
across them).
It is also conceivable that, in some hosts, it is adaptive
for females to oviposit where larvae are forced to partly
chew through sapwood. This forces larvae to tunnel in
straight lines (and thus they do not accidentally cross paths
with neighbors), and allows for females to lay eggs right
next to each other, if tighter egg packing is advantageous.
A test of this hypothesis would be to compare related
species with different egg arm orientations, transverse vs.
longitudinal. Egg spacing (eggs per mm gallery) should
be “tighter” (i.e., a higher number of eggs/mm) in species
with transverse galleries.
4.3.2 Placement of Eggs
Most commonly, including among most basal taxa, eggs are
placed in niches (egg-sized pockets) along both sides of an
egg tunnel. Though usually these are evenly spaced on
either side, some species (such as Dendroctonus simplex
LeConte: Hopkins, 1909) alternate laying several eggs on
one side. In species in which tunnels characteristically
curve strongly, eggs are placed exclusively on the outer side
118 Bark Beetles
of the curve. But also when generally straight or mildly
curved tunnels curve more strongly, eggs will be placed
only on the outer side. In at least some species, but possibly
all or most, phloeophagous females seem to be able to
adjust their egg placement adaptively. For example, Pseu-
doips mexicanus (Hopkins) tunnels are usually curved but
can be straight; eggs are laid on both sides if straight, but
just the outer side if curved (Smith et al., 2009). An
advantage of a curved gallery is that larvae emanating from
the outer side can fan out, reducing the chance of acciden-
tally coming in contact with each other (though two cases of
incidental cannibalism were seen by Smith et al. (2009)).
The vast majority of phloeophagous species construct
egg-sized niches, and lay just one egg in a niche. Interest-
ingly, a few scattered instances of multiple eggs per niche
have evolved: examples include Chaetophloeus hetero-
doxus (Casey) (Swaine, 1918); Pseudoips (Trimble, 1924;
Chamberlin, 1958;S. L. Wood, 1982;Smith et al., 2009;
Zhang et al., 2010); Orthotomicus caelatus (Eichhoff)
(Swaine, 1918); and Liparthrum mexicanum Wood
(Atkinson and Equihua-Martı
´nez, 1985b). Such egg
pockets are wider and deeper than normal egg niches,
and may contain a few eggs (e.g., 1–4 in Pseudoips)or
many (e.g., 6–12 in C. heterodoxus).
Furthermore, some species deposit eggs in widened
portions of the egg tunnel rather than in single egg niches
or egg pockets. Examples include Dendroctonus pse-
udotsugae Hopkins, D. piceaperda Hopkins, D. rufipennis
(¼D. engelmanni Hopkins), D. micans,D. punctatus,
D. valens,D. terebrans (Olivier), Hylurgops pinifex (Fitch),
Dryocoetes americanus Hopkins (¼D. autographus (Rat-
zeburg)), and Orthotomicus laricis (F.) (L€
ovendal, 1898;
Hopkins, 1909; Swaine, 1918; Balachowsky, 1949). In
some cases, these are protected by a layer of frass, just
as are normal egg niches. Intermediate between these
grooves and the egg pockets is the pattern of D. simplex,
which places three or four eggs side by side at the bottom
of an elongate shallow pocket or groove (Swaine, 1918),
and Xylechinosomus valdivianus (Eggers), where clusters
of up to 30 eggs are placed in shallow troughs along the
tunnel wall (Ru
¨hm, 1981). Pseudothysanoes dislocatus
(Blackman) seems to have similar behavior (Blackman,
1922). Hylurdrectonus piniarius Schedl lays eggs loose in
frass in indefinite tunnels in the cortex of Araucaria
branches (Brimblecombe, 1953).
The selective advantages of clustering single niches or
laying more than one egg in an egg pocket are not obvious.
At least with regards to egg pockets, there would seem to be
a cost of greater intra-family resource competition when
larvae hatch so close to each other, and a risk of accidental
siblicide. Perhaps clues can be found in the biology of the
inbreeding D. micans, where clustered larval feeding signif-
icantly increases growth (Figure 3.6A). Dendroctonus
micans breed solitarily in trunks of live spruces or other
conifers. Storer et al. (1997) suggest that larval aggregation
might be important in dealing with host defenses. This
hypothesis suggests that egg clustering in phloeophagous
species will be associated with breeding in live (vs. dead)
plant tissues, particularly in hosts with strong chemical
defenses.
5. SOCIAL EVOLUTION
It is not generally known that bark and ambrosia beetles
exhibit an extraordinary diversity of social systems. Higher
forms of sociality have evolved repeatedly in these insects,
and the only eusocial beetle is the platypodine ambrosia
beetle, A. incompertus (Kent and Simpson, 1992). Bark
and ambrosia beetles are also the only social insects with
closely related haplodiploid and diploid social lineages
(Normark et al., 1999; Jordal et al., 2000), which would
allow comparative studies to contribute to the long-debated
role of haplodiploidy for social evolution (Hamilton, 1964;
Bourke, 2011). Unfortunately, our knowledge of the
detailed behaviors of social species is still superficial, as
sociality has rarely been the primary focus of researchers
working with these insects. This is primarily because
studying insect behavior in tunnel systems under the bark
or in the wood of trees is almost impossible. Exciting pro-
gress is now being made, however, because evolutionary
biologists interested in social behavior have discovered
these beetles as an illustrative alternative to classical hyme-
nopteran model systems (Hamilton, 1967, 1978;
Kirkendall, 1983, 1993; Kirkendall et al., 1997; Peer and
Taborsky, 2007; Biedermann et al., 2009, 2011, 2012;
Biedermann and Taborsky, 2011, submitted;Jordal et al.,
2011; Boomsma, 2013), and because several ambrosia
beetles have been successfully reared in artificial media
(Saunders and Knoke, 1967; French and Roeper, 1972b;
Roeper et al., 1980b; Mizuno and Kajimura, 2002;
Biedermann et al., 2009; Lake Maner et al., 2013), which
allows behavioral observations, experimental manipula-
tions, and, due to their often short generation times,
even artificial selection experiments (Biedermann and
Taborsky, submitted).
5.1 Social Behaviors and Ecology of Bark
and Ambrosia Beetles: an Overview
Animal social systems range from simple gregariousness, to
family groups with parental care, to complex cooperative
breeding or eusocial societies with reproductive altruism
(Wilson, 1971; Alexander et al., 1991; Costa, 2006;
Boomsma, 2013). In bark and ambrosia beetles, all these
forms are present: (1) gregarious feeding is typical for the
phloeophagous larval offspring in certain Dendroctonus
species, many cryphalines, Ozopemon, and some phloeo-
phagous and some spermatophagous Coccotrypes species;
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3119
it is the norm for Xyleborini and Platypodinae. Gregari-
ousness of adults is particularly apparent in cooperative
mass attack in some primary Dendroctonus and Ips species,
but also is found during overwintering or maturation
feeding of many species. (2) Parental investment in the
form of brood care by the mother, the father, or both—also
termed “subsociality”—is ancestral for bark and ambrosia
beetles and thus typical for the whole group. (3) Adult off-
spring refrain from dispersal and engage in “alloparental”
brood care of young siblings at the natal nest, which is likely
confined to some ambrosia beetles (see below) and poten-
tially also Coccotrypes species breeding in seeds. Some of
these species may form true beetle “societies” with division
of labor between adult and immature offspring present in
communal tunnel systems. These can be further split into
“facultatively eusocial” or “obligately eusocial” societies,
depending on whether adult offspring refrain temporarily
or permanently from reproduction (Boomsma, 2009). Cur-
rently, we know of three facultatively eusocial (Xyleborinus
saxesenii (Ratzeburg), X. affinis Eichhoff, Trachyostus gha-
naensis Schedl) and one possibly obligately eusocial
ambrosia beetle (A. incompertus), but there are likely more
eusocial species awaiting discovery.
Larvae of phloem-feeding bark beetles construct their
own tunnels in the phloem during feeding and gradually
move away from their maternal tunnel. As larvae also pack
these mines with frass, there is often no physical contact
between the parents and their offspring. This is not true
for all bark beetles, however, as some Dendroctonus species
and also many non-phloem feeders like Hypothenemus and
Coccotrypes species live in communal galleries. Communal
galleries are also present in many ambrosia beetles, but
tunnels may or may not be altered by ambrosial grazing
by larvae and adults. Larvae and adults can move and
interact freely in such galleries. However, this is not true
for all ambrosia beetles; in Camptocerus, Xyloterini and
Corthylini, larvae are separated from each other because
they develop in individual larval niches and do not move
freely in the galleries. Nevertheless, they still closely
interact with their parents that freely move within the gal-
leries. Consequently, as there are many more interactions
between individuals in galleries of many ambrosia beetles
and non-phloem feeders than in galleries of true bark
beetles, the potential for advanced sociality to evolve is
much higher in the first groups (Kirkendall et al., 1997).
5.2 Basic Concepts of Social Evolution
Theory
The evolution of behavior is fundamentally based on max-
imizing the direct fitness of individuals (i.e., individual-
level selection; Alexander, 1974; Clutton-Brock, 2009).
As Darwin (1859) realized, this cannot explain the evolution
of alloparental care and eusociality, however, because the
beneficiaries of care are not offspring of the caregivers
but rather kin to them with varying degrees of relatedness.
This problem was resolved by William Hamilton’s theory of
inclusive fitness (kin selection theory), which incorporates
both the direct and indirect fitness effects of costly
behaviors: an altruistic behavior can evolve if it benefits
the spread of a cooperative gene, not necessarily by self
reproduction (direct fitness), but also through the repro-
duction of relatives bearing that gene (indirect fitness)
(Hamilton, 1964). More precisely, altruism is selected, for
if the genetic relatedness (r) between social partners is
greater than the ratio of fitness costs (c) to the performer
over the fitness benefits (b) to the recipient: r>c/b. Accord-
ingly, social behaviors typically arise in kin groups and
under ecological conditions that yield higher inclusive
fitness gains when remaining in the natal nest.
Ever since the publication of Hamilton’s paper
(Hamilton, 1964), several ecological conditions have been
identified to generally facilitate social evolution across
various animal groups, which can be roughly grouped in
two categories: environmental constraints on solitary
breeding and benefits of philopatry (Korb and Heinze,
2008; Bourke, 2011). Aiding kin becomes a viable alter-
native to breeding oneself when independent breeding is
very costly. Environmental factors that increase the costs
of solitary breeding include high mortality during dispersal,
breeding sites being limiting, and high population densities
(Emlen, 1982). Philopatry (not dispersing before breeding)
can be beneficial if there is an opportunity to inherit the nest
or a possibility of co-breeding (direct fitness benefits), or by
helping related individuals to increase their reproductive
output (indirect fitness benefits) (Stacey and Ligon, 1991).
5.3 Subsociality and Parental Care in Bark
and Ambrosia Beetles
Subsociality is characterized by reproductive investment
of parents beyond egg laying: post-ovipositional care
increasing survival, growth, and development of offspring
(Wilson, 1971). In insects, it has evolved repeatedly, typi-
cally in connection with abundant but ephemeral resources
and high competition or predation pressure (Tallamy and
Wood, 1986). The bark of dead trees is a prime example
of an environment facilitating subsocial life. Wood suitable
for insect attack is unpredictably distributed and difficult to
locate, but offers an abundant, defendable resource, which
may persist for several generations. The physical properties
of woody tissues and plant defenses like resin flow and toxic
chemical metabolites are likely major obstacles for small
larvae, problems more easily overcome with the help of
adult individuals (Hamilton, 1978;Chapters 1 and 5).
Parents can also assist with food provisioning, in particular
by increasing the quality or digestibility of food. By
120 Bark Beetles
inoculating the wood with microorganisms, they can
increase its nitrogen content and can make plant tissues
easier to assess and assimilate. Wood-feeding insects can
only utilize lignocellulosic resources by engaging in sym-
bioses with bacteria, fungi, or protozoa (Tallamy and
Wood, 1986). As parent beetles can significantly reduce
physical and nutritional limitations for their offspring (see
below), it is not surprising that wood is one of the most
favorable habitats for the origin of subsociality in insects
as well as of insect–microbe associations (Hamilton,
1978, 1996; Tallamy, 1994; Jordal et al., 2011).
Excavation of tunnels by adults for reproduction is uni-
versal in bark and ambrosia beetles. One or both parents
typically remain in the tunnel system, providing nest pro-
tection and removing frass. This behavior is not common
among other weevils that typically lay their eggs singly
on the outside of plants or in small pre-bored cavities, where
the larvae feed solitarily (Lengerken, 1939). The parental
care of bark and ambrosia beetles is no exception in this
habitat, as subsociality has evolved repeatedly in other
weevil clades that bore in wood, such as Cossoninae and
Conoderinae (Kuschel, 1966; Jordal et al., 2011) and Bos-
trychidae and Ciidae (Hamilton, 1979; Kirkendall,
unpubl.). Parental care takes similar forms in these groups,
being characterized by one or both sexes boring oviposition
tunnels, keeping them free of frass, and protecting them
against predators and competitors (Kuschel, 1966; Jordal
et al., 2011). This suggests that selective factors specific
to wood, like the difficulties faced by immature offspring
mentioned above and pressures from competitors and
natural enemies, have repeatedly selected for adult beetles
which bore oviposition tunnels through the outer bark
instead of laying their eggs freely on the plant surface or
in simple slits. Following the successful excavation of a
tunnel in the phloem, there is no reason for a female to leave
this proto-nest after laying the first egg; tunnel excavation is
energetically costly and the habitat offers a nutritious,
defendable, and abundant food resource, which can support
both her own nutritional needs and those of many more
offspring. Studies on predation pressure within and outside
the gallery are rare, but it is likely that, once under the bark
surface, females are also much safer from predation by
vertebrates and invertebrates alike. Beetles in tunnels are
invisible to foraging vertebrates such as birds or lizards,
and invertebrate wood borer predators like ants or
checkered beetles (Cleridae) preferentially attack adult
beetles on the bark as they have considerable difficulty with
extracting them from tunnels (Wichmann, 1967).
Bark and ambrosia beetle females invest relatively
heavily in individual offspring, via egg provisioning and
maternal care. Eggs are unusually large, ranging from
one-sixth the length of the female’s body in Tomicus pilifer
(Spessivtsev) (Wang, 1981) to one-third the size in
X. affinis (Roeper et al., 1980b), T. populi (Petty, 1977),
and Pagiocerus frontalis (F.) (Yust, 1957). Clutch sizes
are modest (commonly, 70–90 eggs, but often smaller:
Browne, 1961), and some bark beetles (such as those colo-
nizing woody petioles of large leaves) lay fewer than a
dozen eggs (Beaver, 1979b; Jordal and Kirkendall, 1998);
these are among the insects with the lowest recorded
fecundity (Hinton, 1981; Nyland, 1995).
Many males and females commit to one or two breeding
sites (Kirkendall, 1983). For holarctic, outbreeding non-
xylomycetophagous species, it is often reported that females
re-emerge after finishing their first egg tunnel (Kirkendall,
1983); Browne (1961), however, believed that in the humid
tropics, females of most species breed in only one bout.
Pairs often die in their gallery system in species from a
variety of genera: Conophthorus lambertianae Hopkins
(Chamberlin, 1958), Scolytus unispinosus LeConte
(Chamberlin, 1918), Pseudohylesinus nebulosus (LeConte)
(Chamberlin, 1918), Dactylipalpus camerunus Hagedorn
(Browne, 1963), T. populi,Procryphalus mucronatus
(LeConte) (Petty, 1977), and C. columbianus (Milne and
Giese, 1969). Committing strongly to a bout of breeding
selects for increased parental investment (Wilson, 1975;
Tallamy and Wood, 1986). Where it has been investigated,
scolytine beetles as diverse as Dendroctonus,Phloeosinus,
Ips,Hypothenemus,andConophthorus digest (histolyze)
their wing muscles once they have begun breeding
(Chapman, 1956; Reid, 1958; Lekander, 1963; Borden and
Slater, 1969; Morgan and Mailu, 1976; Garraway, 1986;
Robertson and Roitberg, 1998; Lo
´pez-Guille
´net al.,
2011); whether or not Platypodinae do this as well is not
known, and how common the phenomenon is within the Sco-
lytinae is similarly unknown. For females, autolysis of wing
muscles must free up quantities of protein for egg production;
the advantages to males are less clear (Robertson, 1998b).
While some females can regenerate their muscles after a
post-ovipositional period of feeding, in many species most
or all re-emerging females cannot fly, e.g., Dendroctonus
(Lawko and Dyer, 1974; Langor, 1987; Gre
´goire, 1988);
Hypothenemus (Ticheler, 1961; Lo
´pez-Guille
´net al.,
2011); and Phloeosinus (Garraway and Freeman, 1981).
Regeneration in Ips males depends on body size and time
spent in the tunnel system (Robertson, 1998a). Scolytines
that do not regenerate wing muscles can and often do walk
to new sites on the same host to start a second egg tunnel,
though they cannot disperse to new breeding material
(Fuchs, 1907; Reid, 1958; Sauvard, 2004).
In at least some Platypodinae, both sexes lose their tarsal
segments after some weeks in the gallery and are thought to
be incapable of dispersing anew (reviewed in Kirkendall
et al., 1997). Here, commitment to one bout of reproduction
seems assured.
This variation in reproductive strategies reflects
varying optimal solutions to the problem of balancing
the number of eggs laid with investment in offspring being
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3121
produced, and (especially for males) balancing investment
in current vs. future offspring. Over time, breeding
material degrades, intraspecific and interspecific compe-
tition increase, and pressure from parasites and predators
increases. Offspring produced late are smaller and conse-
quently have lower fitness than those produced earlier in
the same host (Kajimura and Hiiji, 1994). At some point,
these factors shift the balance in favor away from laying
more eggs towards either investing more in maternal care,
or departing the brood and attempting further reproduction
elsewhere.
5.3.1 Removing or Packing Frass
The simplest and most widespread form of parental care
common to all bark and ambrosia beetles is clearing frass
from the egg tunnel. Females and their offspring produce
large amounts of frass during tunneling and feeding, which
is pushed back towards the entrance by the mother; it is
expelled from the gallery system by the male, if present,
or by the female, or in some cases packed tightly into the
base of the tunnel. Though modifications exist, frass is typ-
ically shuffled out of the nest by sliding it backwards
beneath their body with the legs and then using their elytral
declivity as a shovel to eject it (Wichmann, 1967). Although
the fitness benefits of frass removal have not been studied,
it is likely highly advantageous, as it is invariably present
in all wood-boring weevils. Apart from enabling free
movements within the gallery (females face forward while
tunneling but must turn around and back up to lay eggs in
newly constructed niches), keeping egg galleries free of
frass likely serves two major purposes: ventilation of the
nest, and nest hygiene by removing potential substrate for
parasites and pathogens (e.g., mites, nematodes, fungi, bac-
teria). Ventilation of phloeophagous tunnels is important
enough that it has been proposed as one possible function
for entrance blocking, nuptial chambers, and especially
holes bored upwards through the bark from the oviposition
tunnels (Swaine, 1918; Blackman, 1922; Morgan, 1998; see
below). Both ventilation and hygiene are especially
important in ambrosia beetles, as fungus cultures grow only
under specific moisture content and are very sensitive to
pathogens (Francke-Grosmann, 1967). Likewise X. saxe-
senii females have been shown not only to shuffle frass
and sawdust outside of the gallery but may also remove
intruding mites, spores of fungal pathogens, and diseased
individuals (Biedermann, 2012).
Although females of almost all species begin by
removing frass, in at least a few species it has a been
observed that, some time after commencing oviposition,
females instead begin packing the frass behind them,
forming an impenetrable plug between the active part of
the egg tunnel and the nuptial chamber or even the tunnel
entrance. Oviposition tunnels become plugged with tightly
packed frass in D. ponderosae (Reid, 1958); some Ips
species (Morgan, 1967; Gouger et al., 1975; Garraway,
1986); and some Pityophthorus species (Blackman,
1922). When frass blocks off the nuptial chamber, females
chew small lateral (sometimes vertical) tunnel extensions in
which they can turn around.
Reid and Roitberg (1994) and Robertson (1998b)
used male removal experiments to study the effects of
male residence on female reproduction in the harem polyg-
ynous I. pini. Males usually remain with females for several
weeks, during most of the time that females are ovipositing.
Reid and Roitberg (1994) found that after only 3 or 4 days,
females breeding without males present had laid 11% fewer
eggs. Robertson (1998b) found that there was considerably
more frass in the tunnels of females in systems with
no male, and that females with no male present laid fewer
eggs and produced fewer emerging offspring. Kirkendall
et al. (1997) reported similar effects of frass-removing
males on female reproduction in a different harem po-
lygynous species, Pityogenes chalcographus (L.). They
also summarized published field studies on monogynous
Hylesinus,Scolytus (two species), Trypodendron, and
Camptocerus, in which data could be found for both
females breeding with a male present and females breeding
alone. In all cases, females produced many more eggs
when a male was present (Kirkendall et al., 1997). Existing
data, then, though covering relatively few genera and
species, all support the hypothesis that the most important
feature of prolonged male residency is the benefits to off-
spring production of aiding females with frass removal.
5.3.2 Burrow Blocking or Plugging
Males staying with females is likely ancestral in bark and
ambrosia beetles; there are few species (and no entire
genera) of outbreeding Scolytinae or Platypodinae in which
males do not remain at least some days, and they block the
burrow entrance while there (Kirkendall, 1983). Fur-
thermore, male residence and in some cases egg tunnel
guarding, seems to have evolved in unrelated insect groups
in which females tunnel to oviposit, such as passalids, bos-
trychids, ciids, subsocial cockroaches, and lower termites
(Hamilton, 1979; Tallamy, 1994).
However, males are not always present during periods
when it is beneficial to block. In a very few species, males
may or may not guard females after surface copulations, but
stay with females for at most a few days (reviewed in
Kirkendall, 1983); these include species of Dendroctonus
(Reid, 1958), Strombophorus (Schedl, 1960a; Browne,
1963), Scolytus (Gossard, 1913; Blackman, 1922;
Fisher, 1931; McMullen and Atkins, 1962), an Alniphagus
(Borden, 1969), a Pityophthorus (Hedlin and Ruth, 1970),
and a Conophthorus (Mattson, 1980). As far as is known,
P. puberulus is parthenogenetic, and males do not exist
(Deyrup and Kirkendall, 1983). Even in species in which
males do normally stay, some males may leave early or
122 Bark Beetles
die, leaving the female alone. When no males are available
during some or all oviposition, females may either block the
entrance themselves (especially if oviposition is complete),
or plug the entrance solidly with frass mixed with resin or
possibly oral secretions (Kirkendall, 1984; Kirkendall et al.,
1997). Further evidence for the importance of blocking
entrances (even late in the breeding cycle) comes from
the only ambrosia beetle species in the large inbreeding
genus Hypothenemus, i.e., H. curtipennis (Schedl). If an
H. curtipennis mother dies or departs, the entrance is
blocked by adult offspring (Beaver, 1986). In several platy-
podines, males block the entrance with long cylinders of
wood fibers; if these are removed experimentally, they
are rapidly replaced (Jover, 1952; Husson, 1955). Females
or males die blocking the entrance in a number of species
(Kirkendall, 1984), suggesting a role for blocking even late
in the reproductive cycle.
Blocking of the entrance has long been hypothesized to
have a protective function. Burrow blocking was discussed
at length by Blackman (1922). He hypothesized that it
serves to exclude parasites and predators that might oth-
erwise harm eggs and young larvae (see discussion in
Kirkendall et al., 1997) and observed that any disturbance
of the entrance or even the passing of a shadow over the
opening would cause a male deeper in the gallery system
to promptly return to his post. The clearest example of
parental protection was given by Darling and Roberts
(1999), who observed guarding males of the platypodine
Crossotarsus barbatus Chapuis killing planidia larvae of
Monacon robertsi Boucek (Hymenoptera: Perilampidae),
parasitoids that try to enter the galleries. In I. pini male
removal experiments, both Robertson (1998b) and Reid
and Roitberg (1994) found much higher mortality of
females in harems from which males had been removed,
suggesting that male presence indeed has an important pro-
tective effect. To the extent that males staying with females
protect offspring, male residency can be interpreted as
paternal care.
In the case of inbreeding species, blocking by mothers or
daughters may also hinder the intrusion of unrelated males
(Peer and Taborsky, 2005), and in ambrosia beetles with
communally feeding offspring they have been shown to
protect larvae from accidentally leaving the nest (X. saxe-
senii:Biedermann and Taborsky, 2011).
Blocking could also be important for microclimate. By
plugging and unplugging the entrance with their bodies,
individuals can possibly regulate the microclimate within
the nest, which (as argued above) is especially important
in ambrosia beetles. This too, would be a form of paternal
care when carried out by males, as is normally the case
in outbreeding species. Kalshoven (1959) observed male
Scolytoplatypus eutomoides Blandford (an outbreeding
ambrosia beetle) to perform “...pumping movements,
rapidly jerking to and fro...” in the gallery entrance, which
he interpreted to serve the ventilation of the nest.
Prolonged male residency (during which they accrue
fitness benefits from both blocking and frass removal)
could also be favored by intrasexual selection, if males
who leave too soon risk being supplanted by new males,
or if males of harem polygynous species who leave early
forgo opportunities to acquire further mates. However,
there is little support for this hypothesis (Kirkendall
et al., 1997; Robertson, 1998b), and it likely only applies
to the first week or so of gallery construction. Colonization
of new breeding material in most species seems to be
highly synchronized. When aggregation pheromones are
not involved, the attractiveness of colonized breeding
material seems to decline rapidly, and for taxa with
pheromone systems it is often found that “masking” or
“anti-aggregation” pheromones are produced after pairing
(Rudinsky, 1969;D. L. Wood, 1982;Birch, 1984; Borden,
1985). Thus, the likelihood of new males entering an open
tunnel is low after just a few days, and for harem polyg-
ynous species there are few or no new females arriving
after a short period. Thus, in a study of harem polygynous
I. pini,Reid and Roitberg (1994) found just a 4%
replacement rate over 6 days, for gallery systems from
which males had been removed experimentally.
5.3.3 Ventilation Holes
As mentioned above, females of many species chew special
openings to the outside from the egg tunnels, usually
referred to as ventilation holes or ventilation tunnels.
In species that pack frass rather than expelling it, these
must also serve as turning niches. If they do function as
ventilation holes then they likely increase the survivorship
of young larvae, and hence represent maternal care;
however, they also present possible new entry points for
natural enemies. Melnikova (1964) demonstrated experi-
mentally that for Scolytus ratzeburgi Janson breeding in
beech, these holes regulate humidity, after rejecting the
hypothesis that they could be used for copulation. Broods
with sealed ventilation holes were flooded with sap. The
holes were only made by females, and were still being con-
structed or enlarged after the female was finished ovipo-
siting (¼maternal care). The observations of McKnight
and Aarhus (1973) support this view: in two Hylesinus
species breeding in ash, the species breeding in live tissues
(H. californicus (Swaine)) makes ventilation holes, while
the species breeding in dead tissues (H. criddlei (Swaine))
does not.
5.3.4 Fungus Tending as Maternal Care
The most elaborate forms of maternal care are found in
ambrosia beetles. In these, offspring survival and growth
is largely dependent upon female fungus farming. Ambrosia
beetle females plant and maintain a fungal food supply and
hold pathogens in check. During construction of the egg
tunnels, they disseminate fungal spores from their
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3123
mycetangia to the tunnel walls. Subsequent beetle tending
behavior strongly stimulates the growth in unknown ways
(Francke-Grosmann, 1966; Happ et al., 1975, 1976). Cross-
otarsus japonicus Blandford ambrosia beetles with oral
mycetangia have been observed to spread oral secretions
containing fungal spores on other individuals and on tunnel
walls, via grooming and tending (Nakashima, 1971).
The mother’s cleaning and tending activity is essential for
keeping fungal garden pathogens in check and to keep the
ambrosia fungus from overgrowing immobile eggs
and pupae (Hadorn, 1933;L. R. Batra, 1966; Francke-
Grosmann, 1967; Biedermann and Taborsky, 2011). Oral
applications of secretions to pathogen-infested areas by D.
rufipennis females (not an ambrosia beetle) have clear anti-
microbial effects (Cardoza et al., 2006b). In ambrosia
beetles of the tribe Xyleborini, mothers frequently groom
their eggs, larvae, and pupae with their mouth parts and
relocate brood with behaviors similar to shuffling frass
(French and Roeper, 1975; Kingsolver and Norris, 1977a;
Roeper et al., 1980a; Biedermann and Taborsky, 2011). A
remarkable development of relocation behavior is seen in
females of some Crossotarsus species (Platypodinae) that
have deep hollows in the frons, in which they can carry their
eggs (and maybe small larvae) through the tunnel systems
(Browne, 1961; Darling and Roberts, 1999). Finally, there
are hints of active food provisioning in Monarthrum fas-
ciatum (Say) and Gnathotrichus species (Scolytinae), in
which larvae live in separate niches, where females have
been observed to feed them with pieces of fungal mycelium
(Hubbard, 1897; Doane and Gilliland, 1929).
5.3.5 Paternal Care
The benefits of prolonged male residency can be attributed
to a mixture of sexual and natural selection, as indicated
above. Some of the consequences of burrow blocking and
frass removal increase the number of offspring, and some
increase the survival of those offspring and hence can be
considered paternal care. Paternal care is rare in insects
and hence is of special interest; in the vast majority of
species, males leave females after copulating with them
and are not present when eggs are laid, precluding the evo-
lution of males contributing directly to offspring survi-
vorship. Given that mate abandonment is the norm, it is
striking that male postcopulatory residency is so common
in bark and ambrosia beetles and that male residency seems
to significantly increase offspring survivorship as well as
male fecundity (Kirkendall 1983; Reid and Roitberg,
1994, 1995; Kirkendall et al., 1997; Lissemore, 1997;
Robertson, 1998a, b; Robertson and Roitberg, 1998).
In I. pini,Robertson (1998b) found that the longer that
males stay with females, the more eggs are laid, the longer
the female egg tunnels are, and the less competition there is
between larval progeny thus increasing offspring
survivorship. Such paternal care has long-lasting effects,
as competition during larval development affects adult size;
larger males attract more females (Robertson and Roitberg,
1998) and larger males and females produce larger broods
(Foelker and Hofstetter, 2014). Experimental male removal
in this species also had dramatic effects on increased pre-
dation by tenebrionid and colydiid beetles (Reid and
Roitberg, 1994).
Thus, evidence from I. pini,Crossotarsus, and Scolyto-
platypus supports interpreting male residence as being a
form of paternal care. It is not at all clear yet if this con-
clusion applies more generally. As emphasized by
Kirkendall et al. (1997), male residence is a key feature
of almost all bark and ambrosia beetle mating systems,
and the vast majority of outbreeding species are monog-
ynous. Is male residency selected more strongly by sexual
or natural selection? Comparative studies in genera with
large variation in male behavior (such as in Scolytus, which
includes a few species with no male residency at all) could
provide key insights into the features selecting for and
against postcopulatory residency, and the extent to which
paternal care is a significant factor in species in which
males stay for all or most of a female’s reproduction.
The variability and evolution of male residency is dis-
cussed in detail in Kirkendall (1983) and in Kirkendall
et al. (1997). There is little support in general for the
hypothesis that males remain to increase their own mating
success via mate guarding or attracting further females. Mate
guarding, however, may be important in species in which
males leave before oviposition commences; more impor-
tantly, mate guarding may have been the initial selective
advantage to remaining some time with females after copu-
lating with them. Mate guarding is posited to have preceded
evolution of offspring care in other insects (Tallamy, 1994;
Costa, 2010), and this is likely the case for bark and ambrosia
beetles. Once males are regularly highly related to the off-
spring they are guarding (as would be assured by strict
monogamy or repeated copulations with the same male),
male and female reproductive interests are fully aligned,
and division of labor between the sexes can evolve.
5.3.6 Males in Inbreeders
Despite the importance of males in outbreeding bark and
ambrosia beetles, in inbreeding taxa, the significance of
males for productivity appears to be negligible. Although
all cooperative behaviors that are shown by adult females
other than blocking are also present in male offspring
of X. saxesenii and X. affinis, and all-male colonies (ari-
sing from unfertilized females that lay haploid eggs)
are almost as productive as normal colonies, there are
typically only one to three males per nest. With so few
males present, male behaviors can have little impact on nest
productivity (Biedermann, 2010, 2012; Biedermann and
Taborsky, 2011).
124 Bark Beetles
What selects for diminished roles of males in these taxa?
Sibling mating within subdivided family groups provides an
arena for mate competition between relatives (Charnov,
1982), which favors producing lower numbers of males
(i.e., local mate competition sensu Hamilton, 1967). In
the most extreme cases this may lead to neoteny, as all
resources that would have been utilized by males can be
invested in dispersing females instead (Jordal et al.,
2002). Fighting may be expected among brothers, as in
some sib-mating parasitoid wasps (Hamilton, 1978,
1979), but currently there is no evidence that sibling
fighting takes place in inbreeding bark or ambrosia beetles;
in many species it is extremely unlikely because they reg-
ularly produce only one male per brood, unless broods
become so large that one male may not be able to fertilize
all of his sisters (Kirkendall, 1983, 1993). The pronotal
horns in males of several Xyleborini species (see
Hubbard, 1897), which have been proposed to have a
fighting role (Hamilton, 1979; Costa, 2006), have been
observed to function as hooks to attach to the tunnel wall
during copulation in X. affinis males (Biedermann, 2012).
The only exception might be species with less biased sex
ratios, in which male dispersal and outbreeding occurs reg-
ularly (D. micans,D. punctatus:Section 4.2). The possi-
bility remains that the unusually large males of some
inbreeders, or hooks or horns on inbreeding males, might
be important in competition with unrelated, intruding
males, but little is known as yet of how often unrelated
males successfully enter nests and inseminate non-sisters.
5.4 Delayed Dispersal and
Alloparental Care
The evolution of parental care given by siblings (a form of
alloparental care) requires that generations overlap, i.e., that
immatures are still present when the first offspring reach
adulthood, and that caring for related juveniles for some time
results in higher inclusive fitness than dispersing immedi-
ately and producing own offspring. The first stage in the evo-
lution of alloparental care, given overlap of generations, is
delayed dispersal. Once adults are present in the nest because
they have delayed leaving, there is a potential for evolving to
aid the reproductive efforts of their mother. No new behavior
need evolve, beyond not dispersing or delaying dispersal:
simply by carrying out the same behaviors they would nor-
mally employ while breeding themselves (burrow blocking,
frass removal, fungus tending), they can increase the survi-
vorship of their mother’s family and perhaps increase their
mother’s total reproductive output as well by relieving her
of some of her duties. Because bark and ambrosia beetles
produce large eggs over a period of weeks or even months,
overlap of generations is universal, so the potential for the
evolution of alloparental care is high. What factors might
create delayed dispersal, and can delayed dispersal lead to
significant alloparental care giving? What do we know about
the costs and benefits of delayed dispersal for young adults?
Can non-dispersing individuals breed further in the same
host material?
5.4.1 Delayed Dispersal
Any plant tissues break down once dead, but wood degrades
slowly, and woody tissues can potentially support several
generations of wood-boring insects. The wood of live trees,
however, is well protected, and can potentially support
insect colonies as long as the tree lives. Dead wood, even
in small branches, is a very large resource unit for tiny
beetles, but one that is scattered and unpredictable in the
environment. For scolytines and platypodines, locating
new breeding material is energetically costly and associated
with high levels of mortality. Dead wood degrades slowly
but surely, with the rate of deterioration of individual
resource units depending on the temperature and what other
organisms have colonized the wood. Inner bark degrades
much more rapidly than sapwood so more advanced forms
of social behavior are more likely to evolve in xylomyceto-
phagous species than phloeophagous species. Unconsumed,
usable woody food resources are often still available for
further breeding, even while offspring of the current brood
are still maturing. Young adult beetles, then, have the
options of (1) remaining in the current tunnel system for
at least some time; (2) extending the current tunnel system
and breeding in it; or (3) leaving and attempting to breed
elsewhere. If they do remain, do they do anything that
increases the survivorship of current juveniles?
Delayed dispersal of adult offspring is not common in
nature, though characteristic of social taxa (Wilson, 1971;
Costa, 2006). Adult offspring of bark and ambrosia beetle
species are commonly observed to remain in the natal
gallery system for days, weeks, or months after maturation
(Fuchs, 1907; Kalshoven, 1962; Kirkendall et al., 1997;
McNee et al., 2000; Peer and Taborsky, 2007; Lo
´pez-
Guille
´net al., 2011; Biedermann et al., 2012).
Direct and indirect fitness benefits at the natal nest can
select for prolonged delayed dispersal. Delayed dispersal of
females in X. saxesenii is affected by the quality and amount
of ambrosia fungi (Biedermann and Taborsky, submitted).
These gains might be either (1) direct through feeding up
body reserves for later reproduction, through co-breeding
within the natal nest, or through becoming the lone breeder,
or (2) indirect through engaging in brood care and fungus
tending, thus helping relatives to produce more brood
and increasing offspring survivorship. Benefit (2) is espe-
cially relevant in species with extended egg laying periods
of the mother, where adult and immature offspring stages
overlap considerably and brood that is dependent on adult
care are still present when the mother dies (e.g., X. saxe-
senii;Biedermann et al., 2012).
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3125
The delayed dispersal of adult offspring in bark and
ambrosia beetles was recognized by the pioneers of bark
beetle research (Ratzeburg, 1839; Eichhoff, 1881;
Hopkins, 1909). Typically, it has been attributed to having
to build up energy reserves before dispersal, and this period
of the life cycle is termed pre-emergence feeding or matu-
ration feeding in these beetles (Eichhoff, 1881; Botterweg,
1982; McNee et al., 2000). Other reasons for at least short
delays are adverse environmental conditions (especially
cold temperatures or strong winds) that do not allow dis-
persal or host finding. Typical for poikilothermic animals,
bark and ambrosia beetles are only active above certain
temperatures and the favorable season for host finding of
temperate species is typically in spring or early summer;
the beetles are active year round in subtropical and tropical
forests, barring prolonged dry seasons. Hence, adults often
hibernate within their natal galleries instead of dispersing
immediately after reaching adulthood.
Evidence that maturation feeding promotes delayed dis-
persal comes from phloem-feeding mountain pine beetles,
where females were experimentally prevented from feeding
after molting to adult. They matured normally, but were
less likely to breed successfully, and laid smaller eggs
(Elkin and Reid, 2005). Weather has been repeatedly shown
to limit dispersal: dispersal is facilitated by sunny weather
with little wind, minimum temperatures being in the range
of 10–20 C depending on the species (Bakke, 1968a, 1992;
Salom and McLean, 1989, 1991; Faccoli and Rukalski,
2004) and high air pressure (Biedermann, 2012). Adults
of some species live through unfavorable seasons or
weather periods within their natal nests (other species
survive in leaf litter, under bark of live trees, or in twigs
of live branches).
Although maturation feeding and waiting for favorable
environmental conditions are of primary importance in many
taxa, especially in bark beetles in which individuals feed sep-
arately in their own cradles, it certainly cannot explain the
extraordinarily long philopatric periods of adults in some
ambrosia beetle species. Female ambrosia beetles were
found to lay eggs only after growing their own fungus garden
on which they fed (French and Roeper, 1975; Kingsolver and
Norris, 1977b; Roeper et al., 1980a; Beaver, 1989). Hence, it
is unlikely that reserves accumulated before emergence will
raise the productivity of those beetles sufficiently to out-
weigh the fitness costs of delayed dispersal (the time lost
from potential breeding). In some xyleborine ambrosia
beetles, daughters even remain all their lives within their
natal nests, e.g., X. affinis (Schneider, 1987)andX. saxesenii
(Peer and Taborsky, 2007; Biedermann et al.,2012). Labo-
ratory studies with X. affinis galleries in artificial medium
showed that remaining adult females are fully capable of
breeding independently when they are experimentally
removed from their natal nest (Biedermann et al.,2011),
which suggests that maturation feeding is not essential for
egg laying. Surprisingly, and in contrast to the maturation
feeding hypothesis, delayed dispersal comes at a cost for
females. Xyleborus affinis females that disperse after their
philopatric period produced fewer eggs than females
removed from the gallery before their philopatric period
(Biedermann et al.,2011). This cost may result from co-
breeding or from engaging in alloparental brood care during
the philopatric period at the natal nest.
It is likely that a combination of both direct and indirect
benefits select for delayed dispersal in many ambrosia
beetle species, as (1) ovary dissections revealed that one-
quarter of staying females in X. saxesenii field galleries
(Biedermann et al., 2012) and one-half in X. affinis labo-
ratory galleries (Biedermann et al., 2011) lay eggs in the
natal nest during their philopatric period, and (2) correlative
studies indicate that staying and helping in the nest is trig-
gered by demands of brood dependent on care. The latter
was shown by increased social behavior of staying females
and later dispersal in relation to both increasing numbers of
sibling larvae and pupae (which depend on brood care) and
decreasing numbers of adult “helpers” in both species
(Biedermann et al., 2011; Biedermann and Taborsky,
2011). Numbers of egg layers correlated with neither the
number of staying adult females nor with the number of
eggs, which suggests that egg numbers are regulated and
adjusted to fungus productivity (Biedermann et al., 2012).
A selection experiment on timing of dispersal in X. sax-
esenii showed that delayed dispersal and helping in this
species and are probably genetically linked (Biedermann
and Taborsky, submitted).
Finally, helping in adults can probably evolve relatively
easily, as it seems not to strongly curtail a helper’s future
reproduction because helping is risk free and does not
reduce a helper’s energy stores. The tradeoff between
helping and future reproduction (Queller and Strassmann,
1998; Korb and Heinze, 2008) may thus be weak in such
ambrosia beetles. This may also explain why helping is
even present in male offspring of the haplodiploid X. saxe-
senii and X. affinis. Unexpectedly, recent observations
indicate that they take part in all cooperative behaviors
that are shown by adult females except for blocking
(Biedermann, 2010, 2012; Biedermann and Taborsky,
2011), which suggests that relatedness asymmetries caused
by haplodiploidy, which would favor female-biased help,
are probably offset by inbreeding in these species
(Hamilton, 1972). Nevertheless, because of strong local
male competition, there are only one or two males and up
to 80 females per gallery, and thus their help is of minor
importance.
Several factors disfavor the evolution of delayed dis-
persal of adult offspring, even when food conditions would
allow adult offspring to establish a second generation at
the natal nest site (Gandon, 1999): (1) a buildup during
the breeding period of predators, parasites (e.g., mites,
126 Bark Beetles
nematodes, parasitoids) and pathogens (e.g., fungal sap-
robes) (Dahlsten, 1982; Hofstetter et al., 2006; Cardoza
et al., 2008; Hofstetter and Moser, 2014); (2) problems in
relation to inbreeding, if unrelated mates are not available
(Thornhill, 1993; Gandon, 1999); (3) competition among
closely related individuals (Kirkendall et al., 1997;
West et al., 2002); and (4) the relatively small potential
for indirect fitness benefits at the natal nest for beetles
that live within their food compared to other social insects
that need to forage for their food (Mueller et al., 2005;
Biedermann, 2012).
These four factors may all present serious obstacles that
might often hinder the evolution of forms of sociality
beyond parental care, although the importance of these
factors has not been studied in bark and ambrosia beetles.
Consequently, bark and ambrosia beetle social systems
exceeding subsociality must have evolved mechanisms to
overcome or handle these obstacles. Mechanisms
increasing social immunity (blocking out of predators and
parasites, and gallery hygienic tasks to keep pathogens and
diseases in check), and fungiculture techniques that assure
a long-term food supply, have likely improved in the course
of bark and ambrosia beetle social evolution, as seen in
other fungus-farming social insects (Cremer et al.,2007;
H€
olldobler and Wilson, 2009; Wilson-Rich et al.,2009).
Pseudo-arrhenotoky in H. hampei (Brun et al.,1995a,b;
Borsa and Kjellberg, 1996a, b) and haplodiploidy in the
Xyleborini clade (Normark et al.,1999) may mitigate the
potential hindrance of inbreeding, by allowing the purging
of deleterious mutations through haplodiploid males
(Hamilton, 1967; Smith, 2000).
5.5 Larval Cooperation
Some bark and ambrosia beetles not only have adult helpers
at the natal nest, but can also have larvae that cooperate and
may engage in division of labor with the adults
(Biedermann and Taborsky, 2011). Although data on larval
behavior in these beetles are mostly anecdotic, it could be a
common phenomenon in species with gregariously feeding
offspring and in which adults and larvae can move freely
within their nests. Larval cooperation has been experimen-
tally proven only in the ambrosia beetle X. saxesenii
(Biedermann and Taborsky, 2011), but observations sug-
gesting larval cooperation come also from the phloem
feeding D. micans,D. valens, and D. punctatus (Gre
´goire
et al., 1981; Deneubourg et al., 1990; Furniss, 1995) and
from other ambrosia feeding Xyleborini (X. affinis:
Biedermann, 2012) and Platypodinae, Platypus cylindrus
(F.) (Strohmeyer, 1906), Trachyostus ghanaensis Schedl,
T. aterrimus (Schaufuss), T. schaufussi Schedl (Roberts,
1968), Doliopygus conradti (Strohmeyer), and D. dubius
(Sampson) (Browne, 1963).
Remarkably, this division of labor between adult and
immature stages is almost unique among social insects.
Helper or worker castes in insects without metamorphosis
(Hemimetabola), like aphids or termites, are always
formed by immature individuals, whereas in insects with
metamorphosis (Holometabola), such as beetles and Hyme-
noptera, workers are typically adults, as immature indi-
viduals in ant, wasp, and bee societies are largely
immobile, helpless, and often dependent on adults to be
moved and fed (Wilson, 1971; Choe and Crespi, 1997).
There are very few exceptions of cooperatively behaving
immatures in Hymenoptera, including nest-building-
silk producing weaver ant larvae (Wilson and H€
olldobler,
1980) and nutrient and enzyme producing larvae of
some wasp and ant species (Ishay and Ikan, 1968; Hunt
et al., 1982).
What does larval cooperation in bark and ambrosia
beetles look like? In phloem feeders larvae cooperate pri-
marily by feeding side by side, which helps them to
overcome plant defenses, and aggregation is effected by
pheromones (Gre
´goire et al., 1981; Deneubourg et al.,
1990; Storer et al., 1997). Gregarious feeding is also known
from the ambrosia beetle genus Xyleborinus, in which
larvae feed not only on fungal mycelia (as typical), but
also on fungus-infested wood. Aggregation pheromones
have not been studied in ambrosia beetle larvae, but it is
likely that gregarious feeding may more effectively control
fungal saprobes threatening their primary ambrosia
food fungus (Biedermann, unpubl.; Biedermann and
Taborsky, 2011). Like gregarious feeding on plants, gre-
garious feeding on fungi has been repeatedly found to be
an adaptation of arthropods to overcome the induction of
secondary fungal defenses (Rohlfs, 2005; Rohlfs and
Churchill, 2011).
Larvae take part in gallery hygiene, by relocating frass
and by grooming eggs, pupae, each other, and adults; these
behaviors have been widely reported from different bark
and ambrosia beetle species. In X. saxesenii, larvae
ball up frass, which can then be more easily removed by
their adult siblings (Biedermann and Taborsky, 2011). In
D. micans, larvae pack frass at specific locations, allowing
free movement within the brood chamber (Gre
´goire et al.,
1981); they also block tunnels to hinder access by R. grandis
predators (Koch, 1909). Fifth instar larvae in some Platypo-
dinae also relocate frass to unused gallery parts or for
plugging artificial nest openings (Hadorn, 1933; Beeson,
1941; Kalshoven, 1959) and expel frass and parasitoid pla-
nidia through the nest entrance (Darling and Roberts,
1999). These larvae have a plug-like last abdominal segment,
which can be used both as a shovel and as a device to fully
plug the gallery entrance against intruders (Strohmeyer,
1906). These larvae have been observed to overtake the role
of entrance blocker during times when their parents are deep
inside the nest (Strohmeyer, 1906; Roberts, 1968). In both
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3127
Platypodinae and many Xyleborini, larvae also engage in
excavation of new tunnels or chambers to create more surface
for the developing ambrosia fungus (Strohmeyer, 1906; K ent,
2002; Biedermann and Taborsky, 2011). The flat brood
chambers that are typically found in the genus Xyleborinus
are almost exclusively accomplished by the larval habit of
feeding on fungus-infested wood (Biedermann and
Taborsky, 2011; De Fine Licht and Biedermann, 2012).
The same is true for the long transverse tunnels in nests of
several Platypodinae that are bored by fifth instar larvae
(Roberts, 1962, 1968; Browne, 1972).
The ultimate cause for the larval specialization for
tunneling shown by many ambrosia beetles may relate to
their repeated molting: mandibles of adults gradually wear
down during excavation, and adult females that bore ex-
tensively would suffer from substantial long-term costs.
In contrast, larval mandibles regenerate at each molt
(Biedermann and Taborsky, 2011).
Xyleborinus saxesenii larvae that feed on fungus-
infested wood likely fertilize the growing ambrosia fungus
with the finely fragmented woody sawdust in their feces,
which gets smeared on the gallery walls after defecation
(Hubbard 1897; Biedermann and Taborsky, 2011). This
larval frass probably also contains enzymes for further
wood degradation, as a recent study showed that X. saxe-
senii larvae possess hemicellulases, which are not found
in their adult siblings (De Fine Licht and Biedermann,
2012). Furthermore, bark and ambrosia beetle larvae may
spread associated bacterial and fungal symbionts within
the galleries, which have been shown to have defensive
functions against pathogens, detoxify poisonous plant
metabolites, degrade lignocellulose plant cell walls, or fix
nitrogen from the air (Cardoza et al., 2006b; Adams
et al., 2008; Scott et al., 2008; Morales-Jime
´nez et al.,
2013;Chapter 6). This suggests that cooperation, and
division of labor among larvae and adults, goes far beyond
behavioral interactions, but may also include microbial,
biochemical, and enzymatic processes.
Larval contributions to gallery extension and to hygiene
reduce the workload for adults. Indeed, and against the
common preconception that larvae only compete for
resources among each other, positive effects of larval
numbers on group productivity have been observed in X.
saxesenii (Biedermann and Taborsky, 2011), D. micans
(Storer et al., 1997), and several Platypodinae species, in
which females only lay second egg clutches in the presence
of fifth instar larval helpers (Roberts, 1968).
In summary, larvae in some bark and many ambrosia
beetle species are free to move within the natal nest, and
are not confined to small areas or brood cells like those
of most hymenopteran social societies (Wilson, 1971;
H€
olldobler and Wilson, 1990). This, in combination with
different capabilities of larvae and adults, predisposes espe-
cially ambrosia beetles for division of labor between
larval and adult stages. Importance and specific roles of
larvae in the galleries appear to vary between species
(Biedermann, 2012).
One aspect that has not been studied at all in bark and
ambrosia beetles is the possibility of delayed development
of larvae. If larvae play such an important role in the nests of
many gregarious bark and ambrosia beetle species and there
are possibilities for larvae to gain indirect fitness benefits by
cooperating in the natal nest, selection may favor prolonged
development (e.g., by additional larval instars). Prolonged
development or even permanently immature helper/worker
castes are the rule in hemimetabolous social insects like
termites, aphids, or thrips, in which individuals only mature
to become reproductive queens or kings (Choe and Crespi,
1997; Korb and Heinze, 2008). There are two hints for pro-
longed development also in larvae of bark and ambrosia
beetles. First, the number of larval instars varies between
two and five among species in bark and ambrosia beetles;
it is unknown what factors select for more or fewer instars.
The numbers of instars are sometimes, but not always,
related to size of the adult (Lekander, 1962; Lekander,
1968a, b). Second, among species with helping larvae
(Dendroctonus, Xyleborini, Platypodinae) and for reasons
that remain unclear, there appears to be high variability
in the developmental periods of larvae (Wichmann,
1927). Koch (1909) observed that from D. micans eggs laid
the same day, the progeny pupated over a period of 44 days
without any obvious reasons. While the first larval instars
are typically short and quite fixed in time, the length of
the last instar is highly plastic and in some cases two to four
times longer than all previous instars together (Koch, 1909;
Baker, 1963; Browne, 1963; Biedermann et al., 2009). Gen-
erally, the last instar is typically the one that overtakes most
helping and has evolved even some morphological adapta-
tions for helping (see above). The maximum of five instars
and the longest development of larvae (which can be several
years) relative to the oviposition period of adults are
both found in Platypodinae (Kirkendall et al., 1997). Unfor-
tunately, researchers have rarely reported larval numbers
when dissecting galleries, and experimental studies are
lacking, so prolonged development of larvae as an
investment in siblings must remain speculative.
5.6 The Evolution of Reproductive Altruism
The frequent occurrence of overlapping generations and
cooperative brood care in this group of beetles suggests that
reproductive altruism may be more widespread than cur-
rently known. In Xyleborini, Corthylini, and Platypodinae,
there are several species in which adult females have been
observed to delay reproduction. In a single species,
X. affinis, delayed dispersal and helping at the natal nest
have been experimentally shown to involve fitness costs
128 Bark Beetles
on future independent breeding. Adult daughters remaining
longer in their mother’s nest produced a significantly
smaller brood when given their own choice to breed, than
adult females experimentally removed from the nest before
their delayed dispersal period (Biedermann et al., 2011). As
only some of the females that delayed breeding bred
together with the mother, this implies that helping at the
natal nest is costly for adult females in ambrosia beetles.
Similarly, in X. saxesenii, there are hints that some
daughters remain, never breed, and die within their
mother’s nests (Peer and Taborsky, 2007). Sterile adult
female worker castes seem to be present in A. incompertus
(Harris et al., 1976; Kent and Simpson, 1992), although it
has not yet been fully proven that sterility is non-reversible
in the case when the mother dies (Kirkendall et al., 1997).
Furthermore, while many cooperative behaviors of larvae
and adults are probably relatively inexpensive in terms of
fitness, blocking of the gallery entrance is dangerous and
costly (Kirkendall et al., 1997). Feeding and blocking are
incompatible and blocking individuals have been observed
to be attacked by parasitoids (Beaver, 1986) or killed by
predators (Wichmann, 1967). Hence, blocking can be inter-
preted as self-sacrificing altruism in those Cryphalini, Xyle-
borini, and Platypodinae in which larvae (P. cylindrus:
Strohmeyer, 1906) or non-reproducing adult offspring
(H. curtipennis:Beaver, 1986;X. saxesenii:Biedermann
and Taborsky, 2011;X. germanus: Peer and Taborsky,
2004; A. incompertus:Kent, 2002) have been observed to
take turns in blocking of the nest. This suggests that facul-
tative (or even obligate) eusociality, defined by overlap of
parental and offspring generations, alloparental brood care,
and facultative (or permanent) reproductive altruism of
some individuals (S. W. T. Batra, 1966; Wilson, 1971) have
evolved multiple times in ambrosia beetles.
How is reproductive altruism favored by natural
selection? Similar factors that facilitate the evolution of
alloparental care also predispose for reproductive altruism.
Kin selection is certainly essential, and all current evidence
indicates that altruism can only evolve in groups of rela-
tives, in which individuals invest in the reproduction of
own genes via related individuals (Hamilton, 1964;
Boomsma, 2013). More specifically, studies have shown
that permanently sterile castes can only evolve if colony
foundation is by a single, monogamously mated female,
which assures high relatedness within her offspring group.
This way, relatedness between colony females equals relat-
edness of a female to her own potential offspring; then, any
constraint on individual reproduction can favor the evo-
lution of staying, helping, and ultimately (under the right
conditions) of sterility of helpers (Boomsma, 2009,
2013). Single gallery foundation and monogamy can be
found in some bark beetles and is the rule in ambrosia
beetles (Kirkendall, 1993), which suggests that the precon-
dition for altruism to evolve is present in many species.
There are severe constraints on dispersal and individual
reproduction in bark and ambrosia beetles. Costs of dis-
persal depend on the species, but in general it seems dif-
ficult for beetles to find suitable host trees and establish
galleries (Berryman, 1982). Mortality during dispersal
flight is about 50% for bark beetles (Klein et al., 1978;
Garraway and Freeman, 1981) and 70–80% for an ambrosia
beetle (Milne and Giese, 1970), and survival decreases
rapidly after the first day of host search (Pope et al.,
1980), typically because individuals are exposed to pre-
dation pressure and adverse weather conditions, but also
because they exhaust fat reserves necessary for flying. Suc-
cessful gallery establishment is also difficult as bark and
ambrosia beetles have specific requirements for their
breeding material, like plant taxon, size of material,
moisture content, and the presence or absence of certain
fungi or other microorganisms. Although ambrosia beetles
are typically less specialized to host taxa (Browne, 1958;
Beaver, 1977, 1979a; Atkinson and Equihua-Martı
´nez,
1986b), boring in solid wood, overcoming host tree
defenses (e.g., resins), and planting of fungal cultivars are
risky tasks. Often, less than half of females successfully
manage the last step (Fischer, 1954; Hosking, 1972;
Nord, 1972; Weber and McPherson, 1983; Biedermann
et al., 2009), typically because either the ambrosia fungus
does not grow or fungal pathogens overgrow the initial cul-
tures (Biedermann, 2012; Biedermann et al., 2013). All
these factors render pre-dispersal cooperation and altruism
more profitable, if longevity of the natal gallery allows
adults to gain inclusive fitness benefits.
The longevity of the breeding material is likely the
crucial factor that will affect evolution of cooperation
and reproductive altruism. This depends on competition
with other ambrosia beetles and microorganisms, timing
of beetle attack in the dying process of a tree (in cases where
breeding is in dead hosts), and size and type of host material
that is attacked. Reproductive altruism without sterility can
evolve in species attacking dying or dead trees of large
diameter as long as they provide resources for several gen-
erations of offspring, as seen in X. affinis,X. saxesenii, and
probably other Platypodinae and Xyleborini (see above;
Biedermann, 2012). Facultative suppression of oviposition
assures that females can disperse and breed independently
should the breeding substrate degenerate, and permits
further inclusive fitness gains from helping at the natal nest.
In X. saxesenii, many galleries need to be abandoned after a
single generation, despite the fact that other galleries are
productive for several offspring cycles. Obligate sterility
of adults, however, is expected only to evolve under condi-
tions that consistently provide non-breeding females with
indirect fitness gains. This is the case when beetles colonize
living trees, which can provide food for many consecutive
offspring generations. The only currently known case of
obligate eusociality in beetles is found in A. incompertus,
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3129
which attacks living trees and constructs galleries that may
last for more than 30 years (Kent and Simpson, 1992).
Several more ambrosia beetles breed in living trees, so more
cases of obligate eusociality may be discovered in the future
(Kirkendall et al., 1997). These systems should have
evolved elaborate techniques for maintaining long-term
fungiculture and social immunity, such as mechanisms to
suppress the spread of fungus-garden pathogens and insect
diseases, as have evolved in societies of fungus-farming
ants (Currie, 2001). Unexpected discoveries are likely when
more researchers have started to work with platypodine
ambrosia beetles, especially those in living trees.
6. INTRACELLULAR BACTERIA AND BARK
BEETLE EVOLUTION
Because of their potential influences on the evolution of
bark and ambrosia beetles, we conclude with a brief dis-
cussion of what little we know about intracellular bacteria
in Scolytinae (nothing is known for Platypodinae). Intracel-
lular symbionts in the alpha-proteobacterial genera Wol-
bachia and Rickettsia are widespread in arthropods and
nematodes, with Wolbachia present in 70% of all insects
(Werren et al., 2008). Bark beetles are no exception and
despite the lack of a detailed survey, single screenings have
identified Wolbachia bacteria in Ipini (I. typographus:
Stauffer et al., 1997;P. chalcographus:Arthofer et al.,
2009), Xyleborini (X. germanus:Kawasaki et al., 2010),
Dryocoetini (H. hampei:Vega et al.,2002), and Cryphalini
(Coccotrypes dactiliperda:Zchori-Fein et al., 2006). In the
evolution of insect mating systems, these symbionts are
important, as they have repeatedly been shown to be able
to manipulate host reproductive biology and evolution
(see review by Werren et al., 2008).
Wolbachia, the best studied of these intracellular para-
sites, is vertically transmitted with the egg from an infected
female to her progeny and not via males. Wolbachia has a
variety of phenotypic effects on its host, including (1) fem-
inization (genetic males develop into females); (2) parthe-
nogenesis; (3) selective male killing; and (4) cytoplasmic
incompatibility (prevents infected males from successfully
fertilizing eggs of females that lack the same Wolbachia
types) (Werren et al., 2008). In bark beetles, the role of Wol-
bachia and other intracellular symbionts for host repro-
duction remains largely unstudied.
It would be interesting to determine if extreme sex ratios
in inbreeding Scolytinae are in any way caused by Wol-
bachia infections. This is unlikely, however, given that
the extremely female biased sex ratios in regular inbreeders
are predicted by local mate competition theory, and in most
cases are extremely precise (Hamilton, 1967; Kirkendall,
1983, 1993; Borsa and Kjellberg, 1996a, b; Biedermann,
2010). In the only study on this topic, Zchori-Fein et al.
(2006) found no evidence for an influence of Wolbachia
on sex ratios in C. dactyliperda. Instead, these authors
showed that the elimination of both Wolbachia and Rick-
ettsia by antibiotic treatment led to unfertile females with
no sign of oogenesis. Accordingly, also Xyleborus ferru-
gineus (F.) ambrosia beetles cannot reproduce after elimi-
nation of their unknown intracellular symbionts (Peleg
and Norris, 1973; Norris and Chu, 1980). This may indicate
that Wolbachia have changed their phenotype from repro-
ductive parasitism to obligate mutualism in these inbreeding
scolytids and the hosts are now dependent on the symbionts
for oogenesis and/or nutrition, as clearly shown for other
arthropods (Dedeine et al., 2001; Hosokawa et al.,2010).
However, does Wolbachia also affect the evolution of their
hosts? Generally, there is strong evidence that infections
lead to inbreeding and thus drive speciation (Bordenstein
et al., 2001; Brucker and Bordenstein, 2012). Super-
infection with up to five different Wolbachia strains per
female (Kawasaki et al., 2010) is likely responsible for
smaller broods produced by females mated with males other
than their brothers in the xyleborine ambrosia beetle X. ger-
manus (Peer and Taborsky, 2005). This outbreeding
depression could be caused by cytoplasmic incompatibility,
as egg numbers between outbreeding and inbreeding broods
were equal, but hatching rates differed (Peer and Taborsky,
2005). Whether such outbreeding depression is common in
other inbreeding bark beetles has not been investigated.
Finally, Wolbachia have also been hypothesized to play a
role in the evolution of haplodiploidy in inbreeding taxa
(Normark, 2004). Engelsta
¨dter and Hurst (2006) showed
that paternal genome exclusion, which can be a predecessor
of haplodiploidy, could be caused by cytoplasmic
incompatibility-inducing bacteria in eggs of incompatible
crosses, rendering the embryo functionally haploid. Paternal
genome exclusion as well as Wolbachia are present in H.
hampei (Brun et al., 1995a, b; Vega et al., 2002), which
strongly suggests that the genetic system of bark beetles
may be influenced by intracellular bacterial symbionts.
The abundance and effect of Wolbachia across out-
breeding bark and ambrosia beetle is largely unknown. Wol-
bachia are present in I. typographus (Stauffer et al., 1997)
and P. chalcographus (Arthofer et al., 2009) at low titer
(35.5% of all sampled individuals infected) and at low
density within infected individuals, and no correlation
between infection titer and host population or geographic
location was found. At least for P. chalcographus this sug-
gests either that populations currently evolve towards the
loss of Wolbachia or unidentified fitness advantages con-
serve the infection by the symbiont under certain environ-
mental conditions (Arthofer et al., 2009). Hypothetically,
bark beetle associated fungi may help beetle hosts to cure
themselves from parasitic symbionts (Arthofer et al.,
2009), as these fungi are known to produce a rich array
of antibiotics (Zrimec et al., 2004). It is possible that Wol-
bachia is repeatedly reacquired by the beetles within their
feeding habitat (e.g., Stahlhut et al., 2010).
130 Bark Beetles
7. CONCLUSION
Over 100 million years ago, several early lineages of
weevils began laying eggs in tunnels under bark rather than
in slits cut with their snouts. Two of these, Scolytinae (6000
species) and Platypodinae (1400 species), achieved notable
evolutionary and ecological success. Their shift from an
herbivorous to a saproxylic lifestyle led rapidly to a series
of morphological and behavioral adjustments, adaptations
we also see in a variety of other wood-boring beetles. Sub-
sequent key innovations included male residence and
monogyny, the development of active fungus cultivation,
the evolution of alternative mating systems such as
inbreeding and simultaneous polygyny, and haploidiploidy.
Central was the adoption of living in tunnels within their
food source: tunnels in wood are easily defended, and
encourage long residency, which in turn fosters various ele-
ments of social behavior.
The variation we have documented in this chapter illus-
trates the potential for testing a multitude of general
hypotheses in behavioral ecology and evolutionary biology.
We will soon have the tools to test such hypotheses using
the comparative method. Until very recently, most phyloge-
netic work has been limited in resolution and extent and is
therefore of limited value for this purpose. These problems
will be resolved in the next few years by several current pro-
jects dealing with large-scale weevil and scolytine phyloge-
netics. The 1000-Curculionidae project is based in part on
phylogenomics work using conserved anchored genome
regions; it is expected that most weevil relationships will
be well resolved, including the position of Scolytinae, Pla-
typodinae, and Cossoninae. The same technology is cur-
rently used to develop data matrices for Cryphalini and
Xyleborini, and ultimately to develop further a soon-to-be
published 20-gene phylogeny of Scolytinae (Pistone and
Jordal, in progress).
Hopefully, advances being made by applying the com-
parative method to a broad selection of taxa will be accom-
panied by (or will inspire) complementary experimental
research. From the perspective of evolutionary biology,
four areas discussed in detail in this chapter seem espe-
cially promising for such a combined approach: mating
system evolution, sexual selection, inbreeding, and social
behavior. But in addition, for a topic not covered by us,
we would point out that the application of sound phy-
logenies to existing data on pheromone components will
generate important insights into how pheromone systems
evolve over time, and into the broad question of how such
signaling behavior does or does not constrain the adoption
of new hosts (since some components of pheromones
are modified plant compounds). Analyses such as these
would also point out the major gaps in our knowledge
of bark and ambrosia beetle pheromones: almost nothing
is known, for example, of the pheromone systems of
tropical genera.
7.1 Mating System Evolution
As we have documented, bark and ambrosia beetles provide
behavioral ecologists with multiple origins of mating
systems otherwise rare in invertebrates (and often rare or
nonexistent in vertebrates). Surely, both comparative and
experimental studies of selected Scolytinae (but also of con-
oderine and cossonine weevils with convergent biology)
would contribute considerably to our general understanding
of mating system evolution and allow testing of hypotheses
largely investigated only in birds or fishes. As noted above,
there are genera and even species (or species complexes)
that vary in their mating systems, and that make tempting
targets for such research. There are many abundant and
widespread temperate species that are amenable to research
into the details of monogyny, harem polygyny, and
inbreeding. Phloeophagous and spermatophagous species
in particular are easily reared in the laboratory, and both
fecundity and egg to adult survivorship easily measured.
The fact that most species commonly occur in dense
breeding aggregations makes it easy to gather large
amounts of data and facilitates thorough replication of
experimental treatments (such as removal or addition of
males or females).
7.2 Sexual Selection
Although complete sexual role reversal is rare in insects,
there are surprisingly many cases of males being selective
about which females they mate with. Male mate choice is
believed to occur in at least 58 insect species from 37 fam-
ilies and 11 orders, including I. pini and I. acuminatus,
which we discussed earlier (Bonduriansky, 2001).
Bonduriansky (2001) finds that male choosiness in Cole-
optera is favored, for example, when both sexes occur in
dense aggregations and there are low search costs, a
common scenario for bark and ambrosia beetles. Also
favoring male choosiness is costly male investment
in mating, which could be the case with male-initiated
tunnels and subsequent helping activities. Male choosiness
can evolve if there is large variation in female quality; in
bark beetles, this can be reflected in body size variation
(strongly correlated with fecundity). Investigating the
extent and nature of sex role reversal in Scolytinae and
Platypodinae should be a priority for bark beetle behavioral
ecologists. This should be done both as a broad comparative
study and by the close study of key genera with such vari-
ation (such as Scolytus,Phloeosinus,Hylesinus, and
Pityophthorus + Conophthorus) and species in which role
reversal seems to be actively evolving (e.g., H. varius).
Whether males select females or vice versa is controversial
for I. pini, a common and widespread North American
species deserving further attention in this regard.
We rely heavily on features of the declivity for identi-
fying species of bark and ambrosia beetles, yet we know
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3131
little of the adaptive significance of the enormous variation
we encounter in this key feature. Extreme developments of
sharp points and edges combined with deep declivities
seems to be associated with taking over the nests of other
species, but exactly how such structures are employed is
unknown. It is tempting to attribute more modest variation
in declivity form and ornamentation to sexual selection in
the context of courtship, but there is considerable variation
in the declivities of female Xyleborini as well, all of which
are inbreeders, which as far as is known have only rudi-
mentary courtship and presumably no intersexual selection.
So, the questions arise, how do sexual selection and natural
selection interact in sculpting this part of beetle bodies, in
outbreeding species, and how does the adoption of
inbreeding impact selection on declivities?
7.3 Inbreeding
We have only begun to understand the evolution and
ecology of inbreeding in insects, and in these beetles in par-
ticular. There are several outstanding questions with
regards to Scolytinae that inbreed.
Generally, the distribution of genetic variation (at single
loci, but also variation in combinations of alleles over
several loci) within individuals, families, populations, and
regions has important consequences for the evolutionary
fate and ecological impact of species. Extreme inbreeding
is expected to generate homozygotic genotypes, and small
populations should lose variation among genotypes to
genetic drift. Small amounts of outbreeding, however,
could have enormous consequences. How often do
inbreeders outbreed? How often do males disperse, and
how often do they succeed in entering other nests and
mating with non-sisters? Are matings between non-siblings
“effective” outbreeding: in a local population, what is the
degree of relatedness between females and foreign males?
How are populations of regular inbreeders structured?
Besides these key questions, it is important to investigate
the extent of outbreeding depression in regular inbreeders.
A few genetic studies of inbreeders are mentioned in
Section 4.2, but these only begin to scratch the surface.
We need ecological genetics studies of both indigenous
and invasive species, and of lineages with a wide variety
of ecological specializations.
We repeat that the highly unusual paternal genome loss
system reported for H. hampei has only been demonstrated
for that one species. Taken together with the related
inbreeding genera, this is a lineage of over 200 species. It
would be interesting to know if other inbreeders from
this clade share this rare breeding system.
7.4 Social Evolution
As with inbreeding, we are only beginning to explore the
rich variation in adult and larval social behaviors in these
beetles. Only a few of the many potentially social species
have been studied behaviorally. The most interesting forms
of cooperative behavior seem to be in ambrosia beetles,
but these are particularly difficult to observe since they
tunnel deep in wood. Observing ambrosia beetle behavior
requires establishing them on semi-artificial media in the
laboratory, which is quite labor intensive. The last decade
has seen major advances in the ability to rear and observe
ambrosia beetles, making this group more accessible to
researchers interested in social behavior, and should lead
to the development of several more potential model
systems. Thus far, though, only xyleborine ambrosia beetles
have been reared, and a broader understanding of the
ecology of social behavior in bark and ambrosia beetles will
depend on establishing species from other lineages in the
laboratory.
The relative importance of genetic and ecological
factors in social evolution is still unclear. Scolytinae
and Platypodinae vary in the way they colonize new
breeding material (in large aggregations, or single indi-
viduals), uni- or biparental care, alloparental care by larvae
or adults, and occurrence of division of labor. Further, sub-
social species breed in a wide variety of substrates and
ecosystems.
Fungus farming seems to provide a variety of opportu-
nities for division of labor, hence the repeated evolution of
alloparental care and forms of larval cooperation in
ambrosia beetles. Future research, using well-established
model systems, should investigate the mechanisms by
which these beetles can actively promote the growth of their
fungal cultivars and protect them from pathogens, and can
induce the specialized “ambrosial” growth forms seen in
their tunnels. Careful observations of larvae and adults
can elucidate the roles they each play, and look for previ-
ously unknown expressions of altruistic behavior.
APPENDIX
Larval feeding modes and adult mating systems in Scoly-
tinae, with the total number of species given for each genus.
Rare occurences in a genus (one or a few species) are coded
“(x)” and unknown mating behavior or feeding modes are
indicated by “?”. Abbreviations, larval (and usually adult)
feeding: Phl, phloeophagy (feeding in inner bark); Xlm,
xylomycetophagy (farming fungus); Spm, spermatophagy
(feeding in seeds); Myc, feeding on free-living fungi;
Mye, myelophagy (feeding in pith); Xyl, xylophagy
(feeding in wood); Hbv, herbiphagy (feeding in non-woody
plants); feed?, unknown larval feeding habits. Abbrevia-
tions, mating systems: MG, monogyny; HP, harem
polygyny; BG, bigyny; Col, colonial polygyny (several
males and several females in a gallery system); Inbr,
inbreeding; MS?, unknown mating system. The list of tribes
and genera and the numbers of species were compiled by
T. H. Atkinson (see Chapter 2).
132 Bark Beetles
Tribe Genus Phl Xlm Spm Myc Mye Xly Hbv feed? MG HP BG Col Inbr MS? Spp
Amphiscolytini Amphiscolytus ??1
Bothrosternini Akrobothrus ??1
Bothrosternus x (x) 11
Cnesinus x (x) x x 95
Eupagiocerus (x) x ?3
Pagiocerus xx5
Sternobothrus xx 16
Cactopinini Cactopinus xx 21
Carphodicticini Carphodicticus xx1
Craniodicticus x?3
Dendrodicticus ??1
Corthylini Amphicranus x x (x) 66
Araptus x (x) x (x) (x) 172
Brachyspartus ??1
Conophthorus xx13
Corthylocurus xx15
Corthyloxiphus xx21
Corthylus x x (x) 159
Dacnophthorus xx5
Dendroterus xx15
Glochinocerus x2
Gnatharus ??1
Gnatholeptus xx4
Gnathotrichus xx16
Gnathotrupes xx30
Metacorthylus xx13
Microcorthylus xx38
Mimiocurus xxx 15
Monarthrum x x 140
continued
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3133
Tribe Genus Phl Xlm Spm Myc Mye Xly Hbv feed? MG HP BG Col Inbr MS? Spp
Phelloterus xx3
Phloeoterus xx1
Pityoborus xx7
Pityodendron ??1
Pityophthorus x x x x (x) 385
Pityotrichus xx3
Pseudopityophthorus xx27
Sauroptilius ??1
Spermophthorus x?2
Styphlosoma xx4
Tricolus xx50
Urocorthylus ??1
Cryphalini Acorthylus xx6
Allernoporus xx1
Allothenemus ??1
Coriacephilus x?5
Cosmoderes ??20
Cryphalogenes xx 2
Cryphalus x x 190
Cryptocarenus no? (x) x x 16
Eidophelus x?5
Ernocladius LK x 2
Ernoporicus xx15
Ernoporus xx16
Hemicryphalus ?7
Hypocryphalus xx52
Hypothenemus x (x) x x (x) x 183
Margadillius x?x13
Neocryphus ??2
134 Bark Beetles
Periocryphalus xx2
Procryphalus xx3
Ptilopodius x 1? 17
Scolytogenes xx x 107
Stegomerus xx7
Stephanopodius xxx 6
Trischidias xx7
Trypophloeus xx17
Crypturgini Aphanarthrum x x (x) 29
Cisurgus xx 9
Crypturgus xx15
Deropria x (x) ? 1
Dolurgus xx1
Diamerini Acacicis xx11
Bothrosternoides ??1
Diamerus xx34
Peronophorus xx5
Pseudodiamerus xx3
Sphaerotrypes xx47
Strombophorus xxx 31
Dryocoetini Chiloxylon ??1
Coccotrypes x x x x 129
Cynanchophagus ?1
Cyrtogenius x x x x 106
Dactylotrypes xx1
Dendrocranulus xx 43
Dryocoetes (x) x (x) 37
Dryocoetiops xx?18
Lymantor xx 4
Ozopemon xx21
continued
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3135
Tribe Genus Phl Xlm Spm Myc Mye Xly Hbv feed? MG HP BG Col Inbr MS? Spp
Peridryocoetes ??6
Pseudothamnurgus ?5
Taphronurgus x1
Taphrorychus xx19
Thamnurgus x33
Tiarophorus ??8
Triotemnus x?15
Xylocleptes xx 26
Hexacolini Gymnochilus xx9
Microborus xx8
Pycnarthrum xx18
Scolytodes x (x) (x) x x 207
Hylastini Hylastes xx32
Hylurgops xx21
Scierus xx2
Hylesinini Alniphagus xx3
Cryptocurus ??1
Dactylipalpus xx 11
Ficicis xx14
Hapalogenius x?32
Hylastinus xxx4
Hylesinopsis x (x) x 16
Hylesinus x x (x) 37
Kissophagus xx3
Longulus xx1
Neopteleobius x?1
Phloeoborus ?x x 27
Pteleobius xx2
Rhopalopselion xx 11
136 Bark Beetles
Hylurgini Chaetoptelius xx7
Dendroctonus x x (x) 20
Dendrotrupes x?2
Hylurdrectonus xx4
Hylurgonotus xx 4
Hylurgopinus xx1
Hylurgus xx3
Pachycotes xx 9
Pseudohylesinus xx13
Pseudoxylechinus xx9
Sinophloeus x?1
Tomicus xx7
Xylechinosomus x 11
Xylechinus xxx40
Hyorrhynchini Hyorrhynchus xx11
Pseudohyorrhynchus xx3
Sueus xx5
Hypoborini Chaetophloeus xx24
Cryphyophthorus ??2
Dacryostactus xx1
Glochiphorus ??2
Hypoborus xx2
Liparthrum xxx37
Styracoptinus xx4
Trypanophellos ?1
Zygophloeus ??1
Ipini Acanthotomicus x (x) (x) x 94
Dendrochilus x?9
Ips xx45
Orthotomicus xx20
continued
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3137
Tribe Genus Phl Xlm Spm Myc Mye Xly Hbv feed? MG HP BG Col Inbr MS? Spp
Pityogenes xx24
Pityokteines xx10
Premnobius xx23
Premnophilus xx2
Pseudips xx3
Micracidini Afromicracis ??17
Hylocurus (x) x (x) x 78
Lanurgus xxx22
Micracis xx26
Micracisella xx 20
Miocryphalus x (x) ?
Phloeocleptus xx11
Phloeocurus x?1
Pseudomicracis xxx8
Pseudothysanoes x (x) (x) x 92
Saurotocis xx2
Stenoclyptus xx2
Stevewoodia ??1
Thysanoes xx15
Phloeosinini Asiophilus ??2
Carphotoreus xx1
Catenophorus ??1
Chramesus x (x) (x*) (x) x (x) 92
Cladoctonus xx14
Cortisinus ??1
Dendrosinus xx 7
Hyledius x x (x) 24
Hyleops xx1
Microdictica ??1
138 Bark Beetles
Phloeocranus xx1
Phloeoditica xx2
Phloeosinopsioides ??3
Phloeosinus x(x*) x (x) 66
Pseudochramesus xx11
Phloeotribini Aricerus xx3
Dryotomicus ??4
Phloeotribus x x (x) 103
Phrixosomatini Phrixosoma xx25
Polygraphini Bothinodroctonus x?3
Cardroctonus ??3
Carphobius xx3
Carphoborus xx34
Chortastus xxx5
Dolurgocleptes ??2
Halystus x?2
Polygraphus x (x) x 100
Serrastus xx2
Scolytini Camptocerus xx31
Ceratolepsis xx7
Cnemonyx xx23
Loganius xx16
Scolytopsis xx6
Scolytus x x (x) (x) 126
Scolytoplatypodini Remansus x?4
Scolytoplatypus xx49
Xyleborini Amasa xx41
Ambrosiodmus xx80
Ambrosiophilus xx8
Ancipitis xx1
continued
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3139
Tribe Genus Phl Xlm Spm Myc Mye Xly Hbv feed? MG HP BG Col Inbr MS? Spp
Anisandrus xx14
Arixyleborus xx32
Beaverium xx7
Cnestus xx32
Coptoborus xx23
Coptodryas xx36
Cryptoxyleborus xx18
Cyclorhipidion xx86
Debus xx16
Diuncus xx17
Dryocoetoides xx25
Dryoxylon xx1
Eccoptopterus xx6
Euwallacea xx45
Fortiborus xx6
Hadrodemius xx3
Immanus x 2
Leptoxyleborus xx6
Microperus xx16
Planiculus xx7
Pseudowebbia xx6
Sampsonius xx22
Schedlia xx6
Stictodex xx2
Streptocranus xx11
Taurodemus xx15
Theoborus xx11
Truncaudum xx7
Wallacellus xx3
140 Bark Beetles
Webbia xx38
Xyleborinus xx76
Xyleborus xx404
Xylosandrus xx39
Xyloctonini Cryphalomimus ??3
Ctonoxylon xx28
Glostatus xx18
Scolytomimus xx14
Xyloctonus xx15
Xyloterini Indocryphalus xx8
Trypodendron xx13
Xyloterinus xx1
*
Feeding and reproductive behavior for Scolytinae genera of the world. For most genera, larval feeding mode and mating system information are in the review of world genera by (Wood, 1986; see also
1982, 2007), or regional works of Beeson (1941),Schedl (1958, 1959,1977), Browne (1961, 1963), and Chararas (1962); overlooked or recent information for poorly known genera or exceptional
species is in Kalshoven (1958), Roberts (1969, 1976),Beaver and L€
oyttyniemi (1985), Noguera-Martı
´nez and Atkinson (1990), and Jordal (2006).
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3141
ACKNOWLEDGMENTS
The taxonomic distributions of feeding behaviors and reproductive
systems would not have been possible without the taxonomic data
compilation kindly supplied by T. H. Atkinson. Roger Beaver, Sarah
Smith, and Anthony Cognato replied promptly to repeated requests for
natural history information, which greatly improved the manuscript.
We thank them and all the others who supplied facts or research
reprints. P.H.W.B. is funded by an SNSF Postdoctoral Research Grant
(P300P3_151134).
REFERENCES
Adams, A.S., Six, D.L., 2007. Temporal variation in mycophagy and prev-
alence of fungi associated with developmental stages of Dendroctonus
ponderosae (Coleoptera: Curculionidae). Environ. Entomol.
36, 64–72.
Adams, A.S., Six, D.L., Adams, S.M., Holben, W.E., 2008. In vitro inter-
actions between yeasts and bacteria and the fungal symbionts of the
mountain pine beetle (Dendroctonus ponderosae). Microb. Ecol.
56, 460–466.
Ahnlund, H., 1996. Saproxylic insects on a Swedish dead aspen. Entomo-
logisk Tidskrift 117, 137–144.
Alexander, R.D., 1974. The evolution of social behavior. Annu. Rev. Ecol.
Syst. 5, 325–383.
Alexander, R.D., Noonan, K.M., Crespi, B.J., 1991. The evolution of euso-
ciality. In: Sherman, P.W., Jarvis, J.U.M., Alexander, R.D. (Eds.), The
Biology of the Naked Mole Rat. Princeton University Press, Princeton,
pp. 1–44.
Alfaro, R.I., Humble, L.M., Gonzalez, P., Villaverde, R., Allegro, G., 2007.
The threat of the ambrosia beetle Megaplatypus mutatus (Chapuis)
(¼Platypus mutatus Chapuis) to world poplar resources. Forestry
80, 471–479.
Amezaga, I., 1997. Forest characteristics affecting the rate of shoot pruning
by the pine shoot beetle (Tomicus piniperda L.) in Pinus radiata
D. Don and P. sylvestris L. plantations. Forestry 70, 129–137.
Anderbrandt, O., Schlyter, F., Birgersson, G., 1985. Intraspecific compe-
tition affecting parents and offspring in the bark beetle Ips typographus.
Oikos 45, 89–98.
Andersen, J., Nilssen, A.C., 1983. Intrapopulation size variation
of free-living and tree-boring Coleoptera. Can. Entomol. 15,
1453–1464.
Andersen, H., Jordal, B., Kambestad, M., Kirkendall, L.R., 2012.
Improbable but true: the invasive inbreeding ambrosia beetle
Xylosandrus morigerus has generalist genotypes. Ecol. Evol.
2, 247–257.
Arthofer, W., Riegler, M., Avtzis, D.N., Stauffer, C., 2009. Evidence for
low-titre infections in insect symbiosis: Wolbachia in the bark beetle
Pityogenes chalcographus (Coleoptera, Scolytinae). Environ.
Microbiol. 11, 1923–1933.
Atkinson, T.H., 2010. New species and records of Cactopinus Schwarz
with a key to species (Coleoptera, Curculionidae, Scolytinae).
ZooKeys. 17–33.
Atkinson, T.H., Equihua-Martı
´nez, A., 1985a. Lista comentada de los
coleo
´pteros Scolytidae y Platypodidae del Valle de Me
´xico. Folia
Entomol. Mexic. 65, 63–108.
Atkinson, T.H., Equihua-Martı
´nez, A., 1985b. Notes on biology and
distribution of Mexican and Central American Scolytidae (Cole-
optera). I. Hylesininae, Scolytinae except Cryphalini and Corthylini.
Coleopterists Bulletin 39, 227–238.
Atkinson, T.H., Equihua-Martı
´nez, A., 1985c. Notes on biology and distri-
bution of Mexican and Central American Scolytidae (Coleoptera). II.
Scolytinae: Cryphalini and Corthylini. Coleopterists Bulletin
39, 355–363.
Atkinson, T.H., Equihua-Martı
´nez, A., 1986a. Biology of the Scolytidae
and Platypodidae (Coleoptera) in a tropical deciduous forest at
Chamela, Jalisco. Mexico. Fla. Entomol. 69, 303–310.
Atkinson, T.H., Equihua-Martı
´nez, A., 1986b. Biology of bark and
ambrosia beetles (Coleoptera, Scolytidae and Platypodidae) of a
tropical rain forest in southeastern Mexico with an annotated checklist
of species. Ann. Entomol. Soc. Am. 79, 414–423.
Atkinson, T.H., Peck, S.B., 1994. Annotated checklist of the bark and
ambrosia beetles (Coleoptera: Platypodidae and Scolytidae) of tropical
southern Florida. Fla. Entomol. 77, 313–329.
Atkinson, T.H., Saucedo Ce
´spedes, E., Martı
´nez Ferna
´ndez, E., Burgos
Solorio, A., 1986. Coleo
´pteros Scolytidae y Platypodidae asociados
con las comunidades vegetales de clima templado y frı
´o en el estado
de Morelos, Me
´xico. Acta Zool. Mex. 17, 1–58 (ns).
Ausmus, B.S., 1977. Regulation of wood decomposition rates by arthropod
and annelid populations. Ecol. Bull. 25, 180–192.
Ayres, M.P., Wilkens, R.T., Ruel, J.J., Lombardero, M.J., Vallery, E.,
2000. Nitrogen budgets of phloem-feeding bark beetles with and
without symbiotic fungi. Ecology 81, 2198–2210.
Baker, J.M., 1963. Ambrosia beetles and their fungi, with particular ref-
erence to Platypus cylindrus Fab. In: Mosse, B., Nutman, P.S.
(Eds.), Symbiotic Associations; Thirteenth Symposium of the Society
for General Microbiology. The Syndics of the Cambridge University
Press, London, pp. 232–265.
Bakke, A., 1968a. Ecological studies on bark beetles (Coleoptera: Scoly-
tidae) associated with Scots pine (Pinus sylvestris L.) in Norway with
particular reference to the influence of temperature. Meddelelser
Norske Skogforsøksvesen 21, 441–602.
Bakke, A., 1968b. Field and laboratory studies on sex ratio in Ips acumi-
natus (Coleoptera: Scolytidae) in Norway. Can. Entomol.
100, 640–648.
Bakke, A., 1992. Monitoring bark beetle populations: effects of temper-
ature. J. Appl. Entomol. 114, 208–211.
Balachowsky, A., 1949. Cole
´opte
`res Scolytidae. Libraire de la Faculte des
Sciences, Paris.
Barbey, A., 1901. Les Scolytides de L’Europe Centrale. H. Ku
¨ndig,
Geneva.
Barr, B.A., 1969. Sound production in Scolytidae (Coleoptera) with
emphasis on the genus Ips. Can. Entomol. 101, 636–672.
Barras, S.J., 1973. Reduction of progeny and development in southern pine
beetle following removal of symbiotic fungi. Can. Entomol.
105, 1295–1299.
Batra, L.R., 1963. Ecology of ambrosia fungi and their dissemination by
beetles. Trans. Kansas Acad. Sci. 66, 213–236.
Batra, L.R., 1966. Ambrosia fungi: extent of specificity to ambrosia
beetles. Science 153, 193–195.
Batra, L.R., 1967. Ambrosia fungi—a taxonomic revision and nutritional
studies of some species. Mycologia 59, 976–1017.
Batra, S.W.T., 1966. Nests and social behaviour of halictine bees of India.
Indian J. Entomol. 28, 375–393.
Beal, J.A., Massey, C.L., 1945. Bark beetles and ambrosia beetles (Cole-
optera: Scolytoidea) with special reference to the species occurring in
North Carolina. Duke University School of Forestry Bulletin 10, 1–178.
Beaver, R.A., 1973. Biological studies of Brazilian Scolytidae and Platy-
podidae (Coleoptera) II. The tribe Bothrosternini. Pap. Avulsos Dep.
Zool. 26, 227–236.
142 Bark Beetles
Beaver, R.A., 1976. Biological studies of Brazilian Scolytidae and Platy-
podidae (Coleoptera). 5. The tribe Xyleborini. Z. angew. Entomol.
80, 15–30.
Beaver, R.A., 1977. Bark and ambrosia beetles in tropical forests. Biotrop
Special Publication 2, 133–149.
Beaver, R.A., 1979a. Host specificity in temperate and tropical animals.
Nature 281, 139–141.
Beaver, R.A., 1979b. Leafstalks as a habitat for bark beetles (Col.: Scoly-
tidae). Z. angew. Entomol. 88, 296–306.
Beaver, R.A., 1986. The taxonomy, mycangia and biology of Hypothe-
nemus curtipennis (Schedl), the first known cryphaline ambrosia
beetle (Coleoptera: Scolytidae). Entomol. Scand. 17, 131–135.
Beaver, R.A., 1988. Biological studies on ambrosia beetles of the Sey-
chelles (Col., Scolytidae and Platypodidae). J. Appl. Entomol.
105, 62–73.
Beaver, R.A., 1989. Insect-fungus relationships in the bark and ambrosia
beetles. In: Wilding, N., Collins, N.M., Hammond, P.M., Webber, J.F.
(Eds.), Insect-Fungus Interactions. Academic Press, London,
pp. 121–143.
Beaver, R.A., 2000. Studies on the genus Diapus Chapuis (Coleoptera: Pla-
typodidae) new species and new synonymy. Serangga 5, 247–260.
Beaver, R.A., 2013. The invasive neotropical ambrosia beetle Euplatypus
parallelus (Fabricius, 1801) in the oriental region and its pest status.
The Entomologist’s Monthly Magazine 149, 143–154.
Beaver, R.A., Browne, F.G., 1975. The Scolytidae and Platypodidae (Cole-
optera) of Thailand. A checklist with biological and zoogeographical
notes. Oriental Insects 9, 283–311.
Beaver, R.A., Gebhardt, H., 2006. A review of the Oriental species of Sco-
lytoplatypus Schaufuss (Coleoptera, Curculionidae, Scolytinae).
Dtsch. Entomol. Z. 53, 155–178.
Beaver, R.A., L€
oyttyniemi, K., 1985. Bark and ambrosia beetles
(Coleoptera: Scolytidae) of Zambia. Revue zoologiques africaine
99, 63–85.
Beeson, C.F.C., 1939. New species and biology of Coccotrypes and Tham-
nurgides (Scolytidae, Col.). Indian Forest Records (N. S.). Ento-
mology 5, 279–308.
Beeson, C.F.C., 1941. The Ecology and Control of the Forest Insects of
India and the Neighbouring Countries. The Vasant Press, India.
Benavides, P., Vega, F.E., Romero-Severson, J., Bustillo, A.E., Stuart, J.J.,
2005. Biodiversity and biogeography of an important inbred pest of
coffee, coffee berry borer (Coleoptera: Curculionidae: Scolytinae).
Ann. Entomol. Soc. Am. 98, 359–366.
Bentz, B.J., Six, D.L., 2006. Ergosterol content of fungi associated with
Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera:
Curculionidae, Scolytinae). Ann. Entomol. Soc. Am. 99, 189–194.
Berryman,A.A., 1982. Population dynamics of bark beetles.In: Mitton, J.B.,
Sturgeon, K.B. (Eds.), Bark Beetles in North American Conifers.
A System for the Study of Evolutionary Biology. University of Texas
Press, Austin.
Beukeboom, L.W., Vrijenhoek, R.C., 1998. Evolutionary genetics and
ecology of sperm-dependent parthenogenesis. J. Evol. Biol.
11, 755–782.
Biedermann, P.H.W., 2010. Observations on sex ratio and behavior of
males in Xyleborinus saxesenii Ratzeburg (Scolytinae, Coleoptera).
ZooKeys 56, 253–267.
Biedermann, P.H.W., 2012. The evolution of cooperation in ambrosia
beetles. Ph.D. thesis, University of Bern.
Biedermann, P.H.W., Taborsky, M., 2011. Larval helpers and age poly-
ethism in ambrosia beetles. Proc. Natl. Acad. Sci. U. S. A.
108, 17064–17069.
Biedermann, P. H. W., and Taborsky, M. (submitted). Experimental
social evolution: philopatry and cooperation co-evolve in an ambrosia
beetle.
Biedermann, P.H.W., Klepzig, K.D., Taborsky, M., 2009. Fungus culti-
vation by ambrosia beetles: behavior and laboratory breeding success
in three xyleborine species. Environ. Entomol. 38, 1096–1105.
Biedermann, P.H.W., Klepzig, K.D., Taborsky, M., 2011. Costs of delayed
dispersal and alloparental care in the fungus-cultivating ambrosia
beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae). Behav.
Ecol. Sociobiol. 65, 1753–1761.
Biedermann, P.H.W., Peer, K., Taborsky, M., 2012. Female dispersal and
reproduction in the ambrosia beetle Xyleborinus saxesenii Ratzeburg
(Coleoptera; Scolytinae). Mitteilungen der Deutschen Gesellschaft fu
¨r
allgemeine und angewandte Entomologie 18, 231–235.
Biedermann, P.H.W., Klepzig, K.D., Taborsky, M., Six, D.L., 2013. Abun-
dance and dynamics of filamentous fungi in the complex ambrosia
gardens of the primitively eusocial beetle Xyleborinus saxesenii Rat-
zeburg (Coleoptera: Curculionidae, Scolytinae). FEMS Microbiol.
Ecol. 83, 711–723.
Birch, M.C., 1984. Aggregation in bark beetles. In: Bell, W.J., Carde
´, R.T.
(Eds.), Chemical Ecology of Insects. Chapman and Hall, New York,
pp. 331–353.
Blackman, M.W., 1922. Mississippi bark beetles. Miss., Agric. Exp. Stn.,
Tech. Bull, 11,130 pp., 18 pls.
Blackman, M.W., 1924. The effect of deficiency and excess in rainfall
upon the hickory bark beetle (Eccoptogaster quadrispinosus Say).
J. Econ. Entomol. 17, 460–470.
Blackman, M.W., 1928. The genus Pityophthorus Eichh. in North
America: a revisional study of the Pityophthori, with descriptions of
two new genera and seventy-one new species, 25, New York State
College of Forestry at Syracuse, Technical Publication, 1–184.
Blackman, M.W., 1931. The Black Hills beetle (Dendroctonus ponderosae
Hopk.). Bulletin of the New York State College of Forestry at Syracuse
University 4, 1–97.
Blackman, M.W., Stage, H.H., 1918. Notes on insects bred from the bark
and wood of the American larch, 10,Technical Publication, New York
State College of Forestry at Syracuse University, 1–115.
Blackman, M.W., Stage, H.H., 1924. On the succession of insects living in
the bark and wood of dying, dead and decaying hickory. New York
State College of Forestry at Syracuse University, Technical Publi-
cation 17, 1–268.
Bleiker, K.P., Heron, R.J., Braithwaite, E.C., Smith, G.D., 2013. Preemer-
gence mating in the mass-attacking bark beetle, Dendroctonus pon-
derosae (Coleoptera: Curculionidae). Can. Entomol. 145, 12–19.
Bonduriansky, R., 2001. The evolution of male mate choice in insects: a
synthesis of ideas and evidence. Biol. Rev. 76, 305–339.
Boomsma, J.J., 2009. Lifetime monogamy and the evolution of eusociality.
Philos. Trans. R. Soc., B 364, 3191–3207.
Boomsma, J.J., 2013. Beyond promiscuity: mate-choice commitments in
social breeding. Philos. Trans. R. Soc. B 368,20120050.
Borden, J.H., 1967. Factors influencing the response of Ips confusus
(Coleoptera: Scolytidae) to male attractant. Can. Entomol. 99,
1164–1193.
Borden, J.H., 1969. Observations on the life history and habits of Alni-
phagus aspericollis (Coleoptera: Scolytidae) in southwestern British
Columbia. Can. Entomol. 101, 870–878.
Borden, J.H., 1985. Aggregation pheromones. In: Kerkut, G.A. (Ed.),
Behaviour. Pergamon Press, Oxford, pp. 257–285.
Borden, J.H., Slater, C.E., 1969. Flight muscle volume change in Ips con-
fusus (Coleoptera: Scolytidae). Can. J. Zool. 47, 29–31.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3143
Bordenstein, S.R., O’Hara, F.P., Werren, J.H., 2001. Wolbachia-induced
incompatibility precedes other hybrid incompatibilities in Nasonia.
Nature 409, 707–710.
Borsa, P., Kjellberg, F., 1996a. Experimental evidence for pseudo-
arrhenotoky in Hypothenemus hampei (Coleoptera: Scolytidae).
Heredity 76, 130–135.
Borsa, P., Kjellberg, F., 1996b. Secondary sex ratio adjustment in a pseudo-
arrhenotokous insect, Hypothenemus hampei (Coleoptera: Scoly-
tidae). Comptes Rendus de l’Academie des Sciences Serie Iii-Sciences
de la Vie-Life Sciences 319, 1159–1166.
Botterweg, P.F., 1982. Dispersal and flight behavior of the spruce bark
beetle Ips typographus in relation to sex, size and fat-content.
Z. angew. Entomol. 94, 466–489.
Bourke, A.F.G., 2011. Principles of Social Evolution. Oxford University
Press, Oxford.
Brader, L., 1964.
Etude de la relation entre le scolyte des rameaux du cafe
´ir,
Xyleborus compactus Eichh. (X. morstatti Hag.), et sa planteho
ˆte.
Mededelingen van de Landbouwhogeschool te Wageningen
64, 1–109.
Bright, D.E., 1981. Taxonomic monograph of the genus Pityophthorus
Eichhoff in North and Central America (Coleoptera: Scolytidae).
Mem. Entomol. Soc. Can. 118, 1–378.
Bright, D.E., Poinar Jr., G.O., 1994. Scolytidae and Platypodidae (Cole-
optera) from Dominican Republic Amber. Ann. Entomol. Soc. Am.
87, 170–194.
Bright, D.E., Stark, R.W., 1973. The bark and ambrosia beetles of Cali-
fornia. Coleoptera: Scolytidae and Platypodidae. Bulletin of the Cal-
ifornia Insect Survey 16, 1–169.
Brimblecombe, A.R., 1953. An annotated list of the Scolytidae occurring in
Australia. Queensl. J. Agric. Sci. 10, 167–205.
Browne, F.G., 1958. Some aspects of host selection among ambrosia
beetles in the humid tropics of south-east Asia. Malayan Forest
Records 21, 164–182.
Browne, F.G., 1961. The Biology of Malayan Scolytidae and Platypodidae.
Malayan Forest Records 22, 1–255.
Browne, F.G., 1962. The emergence, flight and mating behaviour of
Doliopygus conradti. West African Timber Borer Research Unit
5, 21–27.
Browne, F.G., 1963. Notes on the habits and distribution of some Ghanaian
bark beetles and ambrosia beetles (Coleoptera: Scolytidae and Platy-
podidae). Bull. Entomol. Res. 54, 229–266.
Browne, F.G., 1965. Types of ambrosia beetle attack on living trees. Proc.
Int. Cong. Entomol. 12, 680.
Browne, F.G., 1968. Pests and Diseases of Forest Plantation Trees. Clar-
endon, Oxford.
Browne, F.G., 1972. Larvae of principal old world genera of Platypodinae.
Trans. R. Entomol. Soc. Lond. 124, 167–190.
Brucker, R.M., Bordenstein, S.R., 2012. Speciation by symbiosis. Trends
Ecol. Evol. 27, 443–451.
Brun, L.O., Borsa, P., Gaudichon, V., Stuart, J.J., Aronstein, K.,
Coustau, C., Ffrench-Constant, R.H., 1995a. ‘Functional’ haplodi-
ploidy. Nature 374, 506.
Brun, L.O., Stuart, J.J., Gaudichon, V., Aronstein, K., Ffrench-
Constant, R.H., 1995b. Functional haplodiploidy—a mechanism for
the spread of insecticide resistance in an important international insect
pest. Proc. Natl. Acad. Sci. U. S. A. 92, 9861–9865.
Cai, Y., Cheng, X., Xu, R., Duan, D., Kirkendall, L.R., 2008. Genetic
diversity and biogeography of red turpentine beetle Dendroctonus
valens in its native and invasive regions. Insect Sci. 15, 291–301.
Campobasso, G., Terragitti, G., Mann, K., Quimby, P.C., 2004. Field and
laboratory biology of the stem-feeding beetle Thamnurgus euphorbiae
(Kuster) (Col., Scolytidae) in Italy, a potential biological control can-
didate of leafy spurge in the USA and Canada. J. Appl. Entomol.
128, 1–5.
Cardoza, Y.J., Paskewitz, S., Raffa, K.F., 2006a. Travelling through time
and space on wings of beetles: a tripartite insect-fungi-nematode asso-
ciation. Symbiosis 41, 71–79.
Cardoza, Y.J., Klepzig, K.D., Raffa, K.F., 2006b. Bacteria in oral secre-
tions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol.
31, 636–645.
Cardoza, Y.J., Moser, J.C., Klepzig, K.D., Raffa, K.F., 2008. Multipartite
symbioses among fungi, mites, nematodes, and the spruce beetle, Den-
droctonus rufipennis. Environ. Entomol. 37, 956–963.
Chamberlin, W.J., 1918. Bark beetles infesting the Douglas fir. Bull.
Oregon Agric. College Exp. Sta. 147, 1–40.
Chamberlin, W.J., 1939. The Bark and Timber Beetles of North America.
North of Mexico, Oregon State College Cooperative Association,
Corvallis, Oregon.
Chamberlin, W.J., 1958. The Scolytoidea of the Northwest: Oregon,
Washington, Idaho, and British Columbia. Oregon State College,
Corvallis.
Chapman, T.A., 1870. On the habits of Platypus cylindrus. Entomologists
Monthly Magazine 7, 103–107, 132–135.
Chapman, J.A., 1956. Flight muscle changes during adult life in a scolytid
beetle, Trypodendron. Nature 177, 1183.
Chararas, C., 1962.
Etude biologique des scolytidae des conife
`res.
P. Lechevalier, Paris.
Charnov, E.L., 1982. The Theory of Sex Allocation. Princeton University
Press, Princeton.
Chodjaı
¨, M., 1963.
Etude e
´cologique de Rugoscolytus mediterraneus
Eggers (Col. Scolytidae) en Iran. Rev. Path. Ve
´g. Entomol. Agr. Fr.
42, 139–160.
Choe, J.C., Crespi, B.J., 1997. The Evolution of Social Behaviour in Insects
and Arachnids. Cambridge University Press, Cambridge.
Chong, J.-H., Reid, L., Williamson, M., 2009. Distribution, host plants, and
damage of the black twig borer, Xylosandrus compactus (Eichhoff), in
South Carolina. J. Agric. Urban Entomol. 26, 199–208.
Civetta, A., Singh, R.S., 1999. Broad-sense sexual selection, sex gene pool
evolution, and speciation. Genome 42, 1033–1041.
Clutton-Brock, T., 2009. Cooperation between non-kin in animal societies.
Nature 462, 51–57.
Cognato, A.I., 2013. Molecular phylogeny and taxonomic review of Pre-
mnobiini Browne 1962 (Coleoptera: Curculionidae: Scolytinae).
Front. Ecol. Evol. 1http://dx.doi.org/10.3389/fevo.2013.00001.
Cognato, A.I., Grimaldi, D., 2009. 100 million years of morphological con-
servation in bark beetles (Coleoptera: Curculionidae: Scolytinae).
Syst. Entomol. 34, 93–100.
Cognato, A.I., Sperling, F.A.H., 2000. Phylogeny of Ips DeGeer species
(Coleoptera: Scolytidae) inferred from mitochondrial cytochrome
oxidase I DNA sequence. Mol. Phylogenet. Evol. 14, 445–460.
Cognato, A.I., Seybold, S.J., Sperling, F.A.H., 1999. Incomplete barriers to
mitochondrial gene flow between pheromone races of the North
American pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Proc.
R. Soc. London B 266, 1843–1850.
Cognato, A.I., Gillette, N.E., Bolan
˜os, R.C., Sperling, F.A.H., 2005. Mito-
chondrial phylogeny of pine cone beetles (Scolytinae, Conophthorus)
and their affiliation with geographic area and host. Mol. Phylogenet.
Evol. 36, 494–508.
144 Bark Beetles
Cognato, A.I., Hulcr, J., Dole, S.A., Jordal, B.H., 2011. Phylogeny of
haplo-diploid, fungus-growing ambrosia beetles (Curculionidae: Sco-
lytinae: Xyleborini) inferred from molecular and morphological data.
Zool. Scr. 40, 174–186.
Costa, J.T., 2006. The Other Insect Societies. Belknapp Press of Harvard
University. Press, Cambridge.
Costa, J.T., 2010. Social evolution in “other” insects and arachnids.
In: Breed, M.D., Moore, J. (Eds.), Encyclopedia of Animal Behavior.
Academic Press, Oxford, pp. 231–241.
Cowling, E.B., Merrill, W., 1966. Nitrogen in wood and its role in wood
deterioration. Can. J. Bot. 44, 1533–1544.
Cremer, S., Armitage, S.A.O., Schmid-Hempel, P., 2007. Social immunity.
Curr. Biol. 17, R693–R702.
Crowson, R.A., 1974. Observations on Histeroidea, with descriptions of an
apterous male, and of the internal anatomy of male Sphaerites.
J. Entomol. Series B, Taxonomy 42, 133–140.
Crozier, R.G., Giese, R.L., 1967a. The Columbian timber beetle, Corthylus
columbianus (Coleoptera: Scolytidae). III. Definition of epiphytotics.
J. Econ. Entomol 60, 55–58.
Crozier, R.G., Giese, R.L., 1967b. The Columbian timber beetle, Corthylus
columbianus (Coleoptera: Scolytidae). IV. Intrastand population dis-
tribution. Can. Entomol. 99, 1203–1214.
Currie, C.R., 2001. A community of ants, fungi, and bacteria: a multilateral
approach to studying symbiosis. Annu. Rev. Microbiol. 55, 357–380.
Dahlsten, D.L., 1982. Relationship between bark beetles and their natural
enemies. In: Mitton, J.B., Sturgeon, K.B. (Eds.), Bark Beetles in North
American Conifers. A System for the Study of Evolutionary Biology.
University of Texas Press, Austin, pp. 140–182.
Dallara, P.L., Seybold, S.J., Meyer, H., Tolasch, T., Francke, W.,
Wood, D.L., 2000. Semiochemicals from three species of
Pityophthorus (Coleoptera: Scolytidae): identification and field
response. Can. Entomol. 132, 889–906.
Darling, D.C., Roberts, H., 1999. Life history and larval morphology of
Monacon (Hymenoptera: Perilampidae), parasitoids of ambrosia
beetles (Coleoptera: Platypodidae). Can. J. Zool. 77, 1768–1782.
Darwin, C., 1859. The Origin of Species. John Murray, London.
De Fine Licht, H.H., Biedermann, P.H.W., 2012. Patterns of func-
tional enzyme activity in fungus farming ambrosia beetles. Front.
Zool. 9, 13.
de Groot, P., Borden, J.H., 1992. Host acceptance behaviour of the jack
pine tip beetle, Conophthorus banksianae and the red pine cone beetle.
C. resinosae. Entomol. Exp. Appl. 65, 149–155.
De Leon, D., 1952. Insects associated with Sequoia sempervirens and
Sequoia gigantea in California. Pan-Pac. Entomol. 28, 75–91.
Dedeine, F., Vavre, F., Fleury, F., Loppin, B., Hochberg, M.E.,
Boule
´treau, M., 2001. Removing symbiotic Wolbachia bacteria specif-
ically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci.
U. S. A. 98, 6247–6252.
Dekle, G.W., Kuitert, L.C., 1968. Orchid insects, related pests and control.
Florida Department of Agriculture, Bulletin of the Division of Plant
Industry 8, 1–28.
Delate, K.M., 1994. Postharvest control treatments for Hypothenemus
obscurus (F.) in macadamia nuts. J. Econ. Entomol. 87, 120–126.
Deneubourg, J.L., Gre
´goire, J.-C., LeFort, E., 1990. Kinetics of larval
gregarious behaviour in the bark beetle Dendroctonus micans (Cole-
optera: Scolytidae). J. Insect Behav. 3, 169–182.
Deyrup, M., 1987. Trischidias exigua Wood, new to the United States,
with notes on the biology of the genus. Coleopterists Bulletin
41, 339–343.
Deyrup, M., Kirkendall, L.R., 1983. Apparent parthenogenesis in
Pityophthorus puberulus (Coleoptera: Scolytidae). Ann. Entomol.
Soc. Am. 76, 400–402.
Doane, R.W., 1923. Leperisinus californicus Sw. killing ash trees. Can.
Entomol. 55, 217.
Doane, R.W., Gilliland, O.J., 1929. Three California ambrosia beetles.
J. Econ. Entomol. 22, 915–921.
Dole, S.A., Jordal, B.H., Cognato, A.I., 2010. Polyphyly of Xylosandrus
Reitter inferred from nuclear and mitochondrial genes (Coleoptera:
Curculionidae: Scolytinae). Mol. Phylogenet. Evol. 54, 773–782.
Duffy, E.A.J., 1968. A monograph of the immature stages of oriental
timber beetles (Cerambycidae). British Museum (Natural History),
London.
Dussourd, D.E., Eisner, T., 1987. Vein-cutting behavior: insect coun-
terploy to the latex defense of plants. Science 237, 898–901.
Eichhoff, W., 1881. Die Europa
¨ischen Borkenka
¨fer. Julius Springer, Berlin.
Eidmann, H.H., 1992. Impact of bark beetles on forests and forestry in
Sweden. J. Appl. Entomol. 114, 193–200.
Elkin, C.M., Reid, M.L., 2005. Low energy reserves and energy allocation
decisions affect reproduction by mountain pine beetles, Dendroctonus
ponderosae. Funct. Ecol. 19, 102–109.
Emlen, S.T., 1982. The evolution of helping. I. An ecological constraints
model. Am. Nat. 119, 29–39.
Emlen, S.T., Oring, L.W., 1977. Ecology, sexual selection, and the evo-
lution of mating systems. Science 197, 215–223.
Engelsta
¨dter, J., Hurst, G.D.D., 2006. Can maternally transmitted endo-
symbionts facilitate the evolution of haplodiploidy? J. Evol. Biol.
19, 194–202.
Entwistle, P.F., 1972. Pests of Cocoa. Longman, London.
Faccoli, M., Rukalski, J.P., 2004. Attractiveness of artificially killed
red oaks (Quercus rubra) to ambrosia beetles (Coleoptera, Scolytidae).
In: Ceretti, P., Hardersen, S., Mason, F., Nardi, G., Tisato, M.,
Zapparoli, M. (Eds.), Invertibrati di una Foresta della Pianura
Padana, Bosco della Fontana. Cierre Grafica Editore, Verona,
pp. 171–179.
Farrell, B.D., Sequeira, A.S., O’Meara, B.C., Normark, B.B., Chung, J.H.,
Jordal, B.H., 2001. The evolution of agriculture in beetles (Curculio-
nidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027.
Felt, E.P., 1914. Notes on forest insects. J. Econ. Entomol. 7, 373–375.
Ferro, M.L., Gimmel, M.L., Harms, K.E., Carlton, C.E., 2009. The beetle
community of small oak twigs in Louisiana, with a literature review of
Coleoptera from fine woody debris. Coleopterists Bulletin
63, 239–263.
Fischer, M., 1954. Untersuchungen u
¨ber den kleinen Holzbohrer
(Xyleborus saxeseni). Pflanzenschutzberichte 12, 137–180.
Fisher, R.C., 1931. Notes on the biology of the large elm bark-beetle, Sco-
lytus destructor Ol. Forestry 5, 120–131.
Flores, L.J., Bright, D.E., 1987. A new species of Conophthorus from
Mexico: descriptions and biological notes. Coleopterists Bulletin
41, 181–184.
Fockler, C.E., Borden, J.H., 1972. Sexual behavior and seasonal mating
activity of Trypodendron lineatum (Coleoptera: Scolytidae). Can.
Entomol. 104, 1841–1853.
Foelker, C.J., Hofstetter, R.W., 2014. Heritability, fecundity, and sexual
size dimorphism in four species of bark beetles (Coleoptera: Curculio-
nidae: Scolytinae). Ann. Entomol. Soc. Am. 107, 143–151.
Forcella, F., 1982. Twig nitrogen content and larval survival of twig-
girdling beetles, Oncideres cingulata (Say) (Coleoptera: Ceramby-
cidae). Coleopterists Bulletin 35, 211–212.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3145
Fox, J.W., Wood, D.L., Akers, R.P., Parmeter, J.R., 1992. Survival and
development of Ips paraconfusus Lanier (Coleoptera, Scolytidae)
reared axenically and with tree–pathogenic fungi vectored by coha-
biting Dendroctonus species. Can. Entomol. 124, 1157–1167.
Fraedrich, S.W., Harrington, T.C., Rabaglia, R.J., Ulyshen, M.D.,
Mayfield, A.E., Hanula, J.L., et al., 2008. A fungal symbiont of the
redbay ambrosia beetle causes a lethal wilt in redbay and other Laur-
aceae in the southeastern United States. Plant Dis. 92, 215–224.
Francke-Grosmann, H., 1956a. Hautdru
¨sen als Tra
¨ger der Pilzsymbiose bei
Ambrosiaka
¨fern. Zeitschrift fu
¨r€
Okologie und Morphologie der Tiere
45, 275–308.
Francke-Grosmann, H., 1956b. Zur U
¨bertragung der Na
¨hrpilze bei Ambro-
siaka
¨fern. Naturwissenschaften 43, 286–287.
Francke-Grosmann, H., 1963a. Die U
¨bertragung der Pilzflora bei dem
Borkenka
¨fer Ips acuminatus. Z. angew. Entomol. 52, 355–361.
Francke-Grosmann, H., 1963b. Some new aspects in forest entomology.
Annu. Rev. Entomol. 8, 415–438.
Francke-Grosmann, H., 1965. Ein Symbioseorgan bei dem Borkenka
¨fer
Dendroctonus frontalis Zimm. (Coleoptera Scolytidae). Naturwis-
senschaften 52, 143.
Francke-Grosmann, H., 1966. U
¨ber Symbiosen von xylo-mycetophagen
und phloeophagen Scolitoidea mit holzbewohnenden Pilzen. Material
und Organismen 1, 503–522, Beiheft.
Francke-Grosmann, H., 1967. Ectosymbiosis in wood-inhabiting beetles.
In: Henry, S.M. (Ed.), Symbiosis. Academic Press, New York,
pp. 141–205.
Francke-Grosmann, H., 1975. Zur epizoischen und endozoischen U
¨ber-
tragung der symbiotischen Pilze des Ambrosiaka
¨fers Xyleborus sax-
eseni (Coleoptera: Scolitidae). Entomologica Germanica 1, 279–292.
French, J.R.J., Roeper, R.A., 1972a. Interactions of ambrosia beetle, Xyle-
borus dispar (Coleoptera, Scolytidae), with its symbiotic fungus
Ambrosiella hartigii (Fungi imperfecti). Can. Entomol.
104, 1635–1641.
French, J.R.J., Roeper, R.A., 1972b. In vitro culture of the ambrosia beetle
Xyleborus dispar (Coleoptera: Scolytidae) with its symbiotic fungus,
Ambrosiella hartigii. Ann. Entomol. Soc. Am. 65, 719–721.
French, J.R.J., Roeper, R.A., 1975. Studies on the biology of the ambrosia
beetle Xyleborus dispar (F.) (Coleoptera: Scolytidae). J. Appl.
Entomol. 78, 241–247.
Fuchs, G., 1907. U
¨ber die Fortpflanzungsverha
¨ltnisse der rindenbru
¨tenden
Borkenka
¨fer verbunden mit einer geschichtlichen und kritischen Dar-
stellung der bisherigen Literatur. Ludwig-Maximilians-University,
Munich, Doctoral Dissertation.
Furniss, M.M., 1995. Biology of Dendroctonus punctatus (Coleoptera:
Scolytidae). Ann. Entomol. Soc. Am. 88, 173–182.
Furniss, M.M., 1996. Taxonomic status of Dendroctonus punctatus
and D. micans (Coleoptera: Scolytidae). Ann. Entomol. Soc. Am.
89, 328–333.
Furniss, M.M., 1997. Conophthorus ponderosae (Coleoptera: Scolytidae)
infesting lodgepole pine cones in Idaho. Environ. Entomol.
26, 855–858.
Gandon, S., 1999. Kin competition, the cost of inbreeding and the evolution
of dispersal. J. Theor. Biol. 200, 345–364.
Garraway, E., 1986. The biology of Ips calligraphus and Ips grandicollis
(Coleoptera: Scolytidae) in Jamaica. Can. Entomol. 118, 113–121.
Garraway, E., Freeman, B.E., 1981. Population-dynamics of the
juniper bark beetle Phloeosinus neotropicus in Jamaica. Oikos
37, 363–368.
Garrick, R.C., Nason, J.D., Fernandez-Manjarres, J.F., Dyer, R.J., 2013.
Ecological co-associations influence species’ responses to past
climatic change: an example from a Sonoran Desert bark beetle.
Mol. Ecol. 22, 3345–3361.
Gascoigne, J., Berec, L., Gregory, S., Courchamp, F., 2009. Dangerously
few liaisons: a review of mate-finding Allee effects. Popul. Ecol.
51, 355–372.
Gast, S.J., Furniss, M.M., Johnson, J.B., Ivie, M.A., 1989. List of Montana
Scolytidae (Coleoptera) and notes on new records. Great Basin Nat.
49, 381–386.
Gianoli, E., Ramos, I., Alfaro-Tapia, A., Valde
´z, Y., Echegaray, E.R.,
Ya
´bar, E., 2006. Benefits of a maize-bean-weeds mixed cropping
system in Urubamba Valley, Peruvian Andes. Int. J. Pest Manage.
4, 283–289.
Gil, Z.N., Bustillo, A.E., Go
´mez, D.E., Marı
´n, P., 2004. Corthylus n. sp.
(Coleoptera: Scolytidae), plaga del aiso en la cuenca del Rı
´o Blanco
en Colombia. Revista Colombiana de Entomologı
´a 30, 171–178.
Gillett, C.P.D.T., Crampton-Platt, A., Timmermans, M.J.T.N., Jordal, B.,
Emerson, B.C., Vogler, A.P., 2014. Bulk de novo mitogenome
assembly from pooled total DNA elucidates the phylogeny of weevils
(Coleoptera: Curculionoidea). Mol. Biol. Evol. http://dx.doi.org/
10.1093/molbev/msu154.
Gime
´nez, R.A., Etiennot, A.E., 2003. Host range of Platypus mutatus
(Chapuis, 1865) (Coleoptera: Platypodidae). Entomotropica
18, 89–94.
Girardi, G.S., Gime
´nez, R.A., Braga, M.R., 2006. Occurrence of Platypus
mutatus Chapuis (Coleoptera: Platypodidae) in a Brazilwood experi-
mental plantation in southeastern Brazil. Neotrop. Entomol.
35, 864–867.
Gobeil, A.R., 1936. The biology of Ips perturbatus Eichhoff. Can. J. Res.
14, 181–204.
Godwin, G., Odell, T.M., 1965. The life history of the white-pine cone
beetle, Conophthorus coniperda. Ann. Entomol. Soc. Am.
58, 213–219.
Goeden, R.D., Norris, D.M., 1965. Some biological and ecological aspects
of ovipositional attack in Carya spp. by Scolytus quadrispinosus
(Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 58, 771–777.
Goldhammer, D.S., Stephen, F.M., Paine, T.D., 1990. The effect of the
fungi Ceratocystis minor (Hedgecock) Hunt, Ceratocystis minor
(Hedgecock) Hunt var. Barrasii Taylor, and SJB 122 on reproduction
of the southern pine beetle, Dendroctonus frontalis Zimmermann
(Coleoptera: Scolytidae). Can. Entomol. 122, 407–418.
Gossard, H.A., 1913. Orchard bark beetles and pin hole borers. Bulletin of
the Ohio Agricultural Experiment Station 264, 1–68.
Gottlieb, D., Holzman, J.P., Lubin, Y., Bouskila, A., Kelley, S.T.,
Harari, A.R., 2009. Mate availability contributes to maintain the
mixed-mating system in a scolytid beetle. J. Evol. Biol.
22, 1526–1534.
Gottlieb, D., Lubin, Y., Harari, A.R., 2014. The effect of female
mating status on male offspring traits. Behav. Ecol. Sociobiol.
68, 701–710.
Gouger, R.J., Yearian, W.C., Wilkinson, R.C., 1975. Feeding and repro-
ductive behaviour of Ips avulsus. Fla. Entomol. 58, 221–229.
Graf, P., 1977. A contribution on the biology and control of Hylesinus
oleiperda F. (Coleopt., Scolytidae) on olive in the Tadla (Morocco).
Z. angew. Entomol. 83, 52–62.
Greco, E.B., Wright, M.G., 2013. Dispersion and sequential sampling plan
for Xylosandrus compactus (Coleoptera: Curculionidae) infesting
Hawaii coffee plantations. Environ. Entomol. 42, 277–282.
Gre
´goire, J.-C., 1988. The greater European spruce bark beetle.
In: Berryman, A.A. (Ed.), Dynamics of Forest Insect Populations. Pat-
terns, Causes, Implications. Plenum, New York, pp. 455–478.
146 Bark Beetles
Gre
´goire, J.-C., Braekman, J.-C., Tondeur, A., 1981. Chemical communi-
cation between the larvae of Dendroctonus micans Kug (Coleoptera:
Scolytidae). Les colloques de l’INRA, 7. Les Me
´diateurs chimiques,
253–257.
Gruner, L., 1974. Biologie et de
´gats d’Hexacolus guyanensis Schedl, dans
les plantations d’acajou rouge (Swietenia macrophylla King.,
Me
´liace
´e) en Guadeloupe (Coleoptera: Scolytidae). Ann. Sci. Forest.
31, 111–128.
Gu
¨clu
¨, C., €
Ozbek, H., 2007. Biology and damage of Thamnurgus pegani
Eggers (Coleoptera: Scolytidae) feeding on Peganum harmala L. in
Eastern Turkey. Proc. Entomol. Soc. Wash. 109, 350–358.
Gue
´rard, N., Dreyer, E., Lieutier, F., 2000. Interactions between Scots pine,
Ips acuminatus (Gyll.) and Ophiostoma brunneo-ciliatum (Math.):
estimation of the critical thresholds of attack and inoculation densities
and effects on hydraulic properties in the stem. Ann. For. Sci.
57, 681–690.
Gurevitz, E., 1975. Contribution a l’e
´tude des Scolytidae I. Comportement
de diffe
´rents stades du scolyte me
´diterrane
´en, Scolytus (Rugoscolytus)
mediterraneus Eggers en Israe
¨l. Annales de zoologie—e
´cologie
animale 7, 477–489.
Haack, R.A., Slansky, F., 1987. Nutritional ecology of wood-feeding
Coleoptera, Lepidoptera, and Hymenoptera. In: Slansky, F.,
Rodriguez, J.G. (Eds.), The Nutritional Ecology of Insects, Mites,
Spiders, and Related Invertebrates. Wiley, New York, pp. 449–486.
Hadorn, C., 1933. Recherches sur la morphologie, les stades evolutifs et
l’hivernage du bostryche lisere (Xyloterus lineatus Oliv.). Beiheft zu
den Zeitschriften des Schweizerischen Forstvereins 11, 1–120.
Hamilton, W.D., 1964. The genetical evolution of social behavior, I and II.
J. Theor. Biol. 7 (1–16), 17–52.
Hamilton, W.D., 1967. Extraordinary sex ratios. Science 156, 477–488.
Hamilton, W.D., 1972. Altruism and related phenomena, mainly in social
insects. Annu. Rev. Ecol. Syst. 3, 193–232.
Hamilton, W.D., 1978. Evolution and diversity under bark.
In: Mound, L.A., Waloff, N. (Eds.), Diversity of Insect Faunas.
Blackwell, Oxford, pp. 154–175.
Hamilton, W.D., 1979. Wingless and fighting males in fig wasps and other
insects. In: Blum, M.S., Blum, N.A. (Eds.), Reproductive Compe-
tition, Mate Choice, and Sexual Selection in Insects. Plenum, New
York, pp. 167–220.
Hamilton, W.D., 1996. Funeral feasts: evolution and diversity under bark.
In: Narrow Roads of Gene Land: The Collected Papers of W. D. Ham-
ilton: Volume 1: Evolution of Social Behaviour. Spektrum Academic
Publishers, Oxford, pp. 387–420.
Hammond, H.E., Langor, D.W., Spence, J.R., 2001. Early colonization of
Populus wood by saproxylic beetles (Coleoptera). Can. J. For. Res.
31, 1175–1183.
Hanavan, R.P., Adams, K.B., Allen, D.C., 2012. Abundance and distri-
bution of peach bark beetle in northern hardwood stands of New York.
N. J. Appl. Forest 29, 128–132.
Hanks, L.M., 1999. Influence of the larval host plant on reproductive strat-
egies of cerambycid beetles. Annu. Rev. Entomol. 44, 483–505.
Hansen, V., 1956. Biller. XVIII Barkbiller. Danmarks Fauna bind 62,
G. E. C. Gads Forlag, Copenhagen.
Hanula, J.L., Mayfield, A.E., Fraedrich, S.W., Rabaglia, R.J., 2008. Biology
and host associations of redbay ambrosia beetle (Coleoptera: Curculio-
nidae: Scolytinae), exotic vector of laurel wilt killing redbay trees in the
southeastern United States. J. Econ. Entomol. 101, 1276–1286.
Happ, G.M., Happ, C.M., Barras, S.J., 1975. Bark beetle fungal symbioses
III. Ultrastructure of conidiogenesis in a Sporothrix ectosymbiont of
the southern pine beetle. Can. J. Bot, 53, 2702–2711.
Happ, G.M., Happ, C.M., Barras, S.J., 1976. Bark beetle fungal symbioses.
II. Fine structure of a basidiomycetous ectosymbiont of the southern
pine beetle. Can. J. Bot. 1049–1062.
Haran, J., Timmermans, M.J.T.N., Vogler, A.P., 2013. Mitogenome
sequences stabilize the phylogenetics of weevils (Curculionoidea)
and establish the monophyly of larval ectophagy. Mol. Phylogenet.
Evol. 67, 156–166.
Harrington, T.C., 2005. Ecology and evolution of mycophagous bark
beetles and their fungal partners. In: Vega, F.E., Blackwell, M.
(Eds.), Insect-Fungal Associations: Ecology and Evolution. Oxford
University Press, New York, pp. 257–295.
Harris, T.W., 1852. A Treatise on some of the Insects of New England which
are Injurious to Vegetation, Second ed. White & Potter, Boston.
Harris, J.A., Campbell, K.G., Wright, G.M., 1976. Ecological studies on
the horizontal borer Austroplatypus incompertus (Schedl) (Coleoptera:
Platypodidae). J. Entomol. Soc. Aust. (N. S. W.) 9, 11–21.
Hedlin, A.F., Ruth, D.S., 1970. A Douglas-fir twig mining beetle, Pity-
pohthorus orarius (Coleoptera: Scolytidae). Can. Entomol.
102, 105–108.
Hedlin, A.F., Yates, H.O., Tovar, D.C., Ebel, B.H., Koerber, T.W.,
Merkel, E.P., 1980. Cone and seed insects of North American conifers.
Environment Canada, Canadian Forest Service, Ottawa.
Heidenreich, E., 1960. Prima
¨rbefall durch Xylosandrus germanus an Jun-
geichen. Anz. Scha
¨dlingskd. 23, 5–10.
Herfs, A., 1950. Studien an dem Steinnußborkenka
¨fer, Coccotrypes tan-
ganus Eggers. H€
ofchen-Briefe fu
¨r Wissenschaft und Praxis 3, 3–31.
Herfs, A., 1959. U
¨ber den Steinnußborkenka
¨fer Coccotrypes dactyliperda
F. Anz. Scha
¨dlingskd. 32, 1–4.
Hinton, H.E., 1981. Biology of Insect Eggs, Vol. 1, Pergamon Press,
New York.
Hofstetter, R.W., Moser, J.C., 2014. The role of mites in insect-fungus
associations. Annu. Rev. Entomol. 59, 537–557.
Hofstetter, R.W., Cronin, J.T., Klepzig, K.D., Moser, J.C., Ayres, M.P.,
2006. Antagonisms, mutualisms and commensalisms affect outbreak
dynamics of the southern pine beetle. Oecologia 147, 679–691.
H€
olldobler, B., Wilson, E.O., 1990. The Ants. The Belknap Press of
Harvard University Press, Cambridge.
H€
olldobler, B., Wilson, E.O., 2009. The Superorganism: The Beauty, Ele-
gance, and Strangeness of Insect Societies. W. W. Norton & Company,
Inc., New York.
Holzman, J., Bohonak, A., Kirkendall, L., Gottlieb, D., Harari, A.,
Kelley, S., 2009. Inbreeding variability and population structure in
the invasive haplodiploid palm-seed borer (Coccotrypes dactyli-
perda). J. Evol. Biol. 22, 1076–1087.
Hopkins, A.D., 1904. Insects injurious to hardwood forests. U.S.
Department of Agriculture, Yearbook for 1903, 313–328.
Hopkins, A.D., 1908. Notable depredations by forest insects. U.S.
Department of Agriculture, Yearbook for 1907, 149–164.
Hopkins, A.D., 1909. Contributions toward a monograph of the scolytid
beetles. I. The genus Dendroctonus, 17 U.S. Department of Agri-
culture, Bureau of Entomology, Technical Bulletin 1–164.
Hopping, G.R., 1964. The breeding evidence indicating two genetic types
of females of Ips tridens. Can. Entomol. 96, 117–118.
Hosking, G.B., 1972. Xyleborus saxeseni, its life-history and flight
behaviour in New Zealand. N. Z. J. For. Sci. 3, 37–53.
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.-Y., Fukatsu, T., 2010. Wol-
bachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl.
Acad. Sci. U. S. A. 107, 769–774.
Howard, T.M., 1973. Accelerated tree death in mature Nothofagus cun-
ninghamii Oerst forests in Tasmania. Victorian Natur. 90, 343–345.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3147
Howard, R.W., Blomquist, G.J., 2005. Ecological, behavioral, and bio-
chemical aspects of insect hydrocarbons. Annu. Rev. Entomol.
50, 371–393.
Hubbard, H.G., 1897. The ambrosia beetles of the United States.
In: Howard, L.O. (Ed.), Some Miscellaneous Results of the Work of
the Division of Entomology, pp. 9–13, U.S. Dept. of Agriculture
Bureau of Entomology Bull. No. 7.
Hulcr, J., Cognato, A., 2010. Repeated evolution of theft in fungus farming
ambrosia beetles. Evolution 64, 3205–3211.
Hulcr, J., Dunn, R.R., 2011. The sudden emergence of pathogenicity in
insect-fungus symbioses threatens naive forest ecosystems. Proc. R.
Soc. B 278, 2866–2873.
Hulcr, J., Mogia, M., Isua, B., Novotny, V., 2007. Host specificity
of ambrosia and bark beetles (Col., Curculionidae: Scolytinae and
Platypodinae) in a New Guinea rainforest. Ecol. Entomol.
32, 762–772.
Hulcr, J., Beaver, R.A., Puranasakul, W., Dole, S.A., Sonthichai, S., 2008a.
A comparison of bark and ambrosia beetle communities in two forest
types in northern Thailand (Coleoptera: Curculionidae: Scolytinae and
Platypodinae). Environ. Entomol. 37, 1461–1470.
Hulcr, J., Novotny, V., Maurer, B.A., Cognato, A.I., 2008b. Low beta
diversity of ambrosia beetles (Coleoptera: Curculionidae: Scolytinae
and Platypodinae) in lowland rainforests of Papua New Guinea. Oikos
117, 214–222.
Hunt, J.H., Baker, I., Baker, H.G., 1982. Similarity of amino-acids in nectar
and larval saliva—the nutritional basis for trophallaxis in social wasps.
Evolution 36, 1318–1322.
Husson, R., 1955. Sur la biologie du Cole
´opte
`re xylophage Platypus
cylindrus Fabr. Annales Univeristatis Saraviensis—Scientia
4, 348–356.
Ishay, J., Ikan, R., 1968. Food exchange between adults and larvae in Vespa
orientalis F. Anim. Behav. 16, 298–303.
Janin, J.L., Lieutier, F., 1988. Early mating in the life-cycle of Tomicus
piniperda L. (Coleoptera, Scolytidae) in the forest of Orleans (France).
Agronomie 8, 169–172.
Janzen, D.H., 1971. Seed predation by animals. Annu. Rev. Ecol. Syst.
2, 465–492.
Janzen, D.H., 1972. Association of a rainforest palm and seed-eating
beetles in Puerto Rico. Ecology 53, 258–261.
Jaramillo, J., Borgemeister, C., Baker, P., 2006. Coffee berry borer
Hypothenemus hampei (Coleoptera: Curculionidae): searching for sus-
tainable control strategies. Bull. Entomol. Res. 96, 223–233.
Jaramillo, J.L., Ospina, C.M., Gil, Z.N., Montoya, E.C., Benavides, P.,
2011. Advances on the biology of Corthylus zulmae (Coleoptera:
Curculionidae) in Alnus acuminata (Betulaceae). Revista Colombiana
de Entomologı
´a 37, 48–55.
Jones, V.P., 1992. Effect of harvest interval and cultivar on damage to
macadamia nuts caused by Hypothenemus obscurus. J. Econ. Entomol.
85, 1878–1883.
Jordal, B.H., 1998. New species of Scolytodes (Coleoptera: Scolytidae)
from Costa Rica and Panama. Rev. Biol. Trop. 46, 407–419.
Jordal, B.H., 2001. The origin and radiation of sib-mating haplodiploid
beetles (Coleoptera, Curculionidae, Scolytinae), PhD thesis,
University of Bergen.
Jordal, B.H., 2006. Community structure and reproductive biology of bark
beetles (Coleoptera: Scolytinae) associated with Macaronesian
Euphorbia shrubs. Eur. J. Entomol. 103, 71–80.
Jordal, B.H., 2013. Deep phylogenetic divergence between Scolytopla-
typus and Remansus, a new genus of Scolytoplatypodini from
Madagascar (Coleoptera, Curculionidae, Scolytinae). ZooKeys 9–33.
Jordal, B.H., 2014a. Cossoninae. In: Leschen, R.A.B., Beutel, R. (Eds.),
Handbook of Zoology, Band IV Arthropoda: Insecta. Part 38: Cole-
optera, Beetles, Vol. 3. de Gruyter, Berlin, pp. 345–349.
Jordal, B.H., 2014b. Platypodinae. In: Leschen, R.A.B., Beutel, R. (Eds.),
Handbook of Zoology, Band IV Arthropoda: Insecta.
Part 38: Coleoptera, Beetles, Vol. 3. de Gruyter, Berlin, pp. 358–364.
Jordal, B.H., 2014c. Scolytinae. In: Leschen, R.A.B., Beutel, R. (Eds.),
Handbook of Zoology, Band IV Arthropoda: Insecta. Part 38: Cole-
optera, Beetles, Vol. 3. de Gruyter, Berlin, pp. 349–358.
Jordal, B., Cognato, A., 2012. Molecular phylogeny of bark and ambrosia
beetles reveals multiple origins of fungus farming during periods of
global warming. BMC Evol. Biol. 12, 133.
Jordal, B.H., Kambestad, M., 2014. DNA barcoding of bark and ambrosia
beetles reveals excessive NUMTs and consistent east-west divergence
across Palearctic forests. Mol. Ecol. Resour. 14, 7–17.
Jordal, B.H., Kirkendall, L.R., 1998. Ecological relationships of a guild of
tropical beetles breeding in Cecropia petioles in Costa Rica. J. Trop.
Ecol. 14, 153–176.
Jordal, B.H., Normark, B.B., Farrell, B.D., 2000. Evolutionary radiation of
an inbreeding haplodiploid beetle lineage (Curculionidae, Scolytinae).
Biol. J. Linn. Soc. 71, 483–499.
Jordal, B.H., Beaver, R.A., Kirkendall, L.R., 2001. Breaking taboos in the
tropics: incest promotes colonization by wood-boring beetles. Glob.
Ecol. Biogeogr. 10, 345–357.
Jordal, B.H., Beaver, R.A., Normark, B.B., Farrell, B.D., 2002. Extraor-
dinary sex ratios and the evolution of male neoteny in sib-mating
Ozopemon beetles. Biol. J. Linn. Soc. 75, 353–360.
Jordal, B.H., Emerson, B.C., Hewitt, G.M., 2006. Apparent “sympatric”
speciation in ecologically similar herbivorous beetles facilitated
by multiple colonizations of an island. Mol. Ecol. 15, 2935–2947.
Jordal, B., Gillespie, J.J., Cognato, A.I., 2008. Secondary structure
alignment and direct optimization of 28S rDNA sequences provide
limited phylogenetic resolution in bark and ambrosia beetles (Curcu-
lionidae: Scolytinae). Zool. Scr. 37, 43–56.
Jordal, B.H., Sequeira, A.S., Cognato, A.I., 2011. The age and phylogeny
of wood boring weevils and the origin of subsociality. Mol. Phylo-
genet. Evol. 59, 708–724.
Jover, H., 1952. Note pre
´liminaire su la biologie des Platypodidae de basse
Co
ˆte d’Ivoire. Revue de pathologie ve
´ge
´tale et d’entomologie agricole
de France 31, 73–81.
Kajimura, H., Hijii, N., 1994. Reproduction and resource utilization of the
ambrosia beetle, Xylosandrus mutilatus, in field and experimental
populations. Entomol. Exp. Appl. 71, 121–132.
Kalshoven, L.G.E., 1925. Primaire aantasting van houtige gewassen door
Xyleborus-soorten. Overdruk uilhet Verslag van de resde Vergadering
van de Vereeniging van Proefstation-personeel Gehouden te Djocja,
7 Oct 1925, 1–14.
Kalshoven, L.G.E., 1958. Studies on the biology of Indonesian Scolytoidea
I. Tijdschr. Entomol. 101, 157–184.
Kalshoven, L.G.E., 1959. Studies on the biology of Indonesian Scolytoidea
II. Tijdschr. Entomol. 102, 135–173.
Kalshoven, L.G.E., 1960a. A form of commensalism occurring in Xyle-
borus species? Entomologische Berichten 20, 118–120.
Kalshoven, L.G.E., 1960b. Studies on the biology of Indonesian Platypo-
didae. Tijdschr. Entomol. 103, 31–53.
Kalshoven, L.G.E., 1962. Note on the habits of Xyleborus destruens Bldf.,
the near-primary borer of teak trees on Java. Entomologische Ber-
ichten 22, 7–18.
Kamata, N., Esaki, K., Kato, K., Igeta, Y., Wada, K., 2002. Potential
impact of global warming on deciduous oak dieback caused by
148 Bark Beetles
ambrosia fungus Raffaelea sp. carried by ambrosia beetle Platypus
quercivorus (Coleoptera: Platypodidae) in Japan. Bull. Entomol.
Res. 92, 119–126.
Kaneko, T., Tamaki, Y., Takagi, K., 1965. Preliminary report on the
biology of some Scolytid beetles, the tea root borer, Xyleborus ger-
manus Blanford, attacking tea roots, and the tea stem borer, Xyleborus
compactus Eichhoff, attacking tea twigs. Japanese Journal of Applied
Entomology and Zoology 9, 23–28.
Kausrud, K.L., Gre
´goire, J.-C., Skarpaas, O., Erbilgin, N., Gilbert, M.,
Økland, B., Stenseth, N.C., 2011. Trees wanted dead or alive! Host
selection and population dynamics in tree-killing bark beetles. PLoS
One 6, e18274.
Kausrud, K., Okland, B., Skarpaas, O., Gre
´goire, J.C., Erbilgin, N.,
Stenseth, N.C., 2012. Population dynamics in changing environments:
the case of an eruptive forest pest species. Biol. Rev. 87, 34–51.
Kawasaki, Y., Ito, M., Miura, K., Kajimura, H., 2010. Superinfection of
five Wolbachia in the alnus ambrosia beetle, Xylosandrus germanus
(Coleoptera: Curculionidae). Bull. Entomol. Res. 100, 231–239.
Keen, F.P., 1958. Cone and Seed Insects of Western Forest Trees.
U.S. Department of Agriculture, Technical Bulletin no. 1169,
Washington, DC.
Kegley, S.J., Furniss, M.M., Gre
´goire, J.-C., 1997. Electrophoretic
comparison of Dendroctonus punctatus LeConte and D. micans
(Kugelann) (Coleoptera: Scolytidae). Pan-Pac. Entomol. 73, 40–45.
Kemner, N.A., 1916. Na
˚gra nya eller mindre ka
¨nda skadedjur pa
˚frukttra
¨d.
Medd. nr. 133 fra
˚n Centralanstalten f€
orF
€
ors€
oksva
¨sendet pa
˚Jordbruk-
somra
˚det, Entomol. avd. nr. 25,21 pp.
Kent, D., 2002. Biology of the ambrosia beetle Austroplatypus incompertus
Aust. J. Entomol. 41, 378.
Kent, D.S., Simpson, J.A., 1992. Eusociality in the beetle Austroplatypus
incompertus (Coleoptera: Platypodidae). Naturwissenschaften
79, 86–87.
Kingsolver, J.G., Norris, D.M., 1977a. The interaction of the female
ambrosia beetle, Xyleborus ferrugineus (Coleoptera: Scolytidae), with
her eggs in relation to the morphology of the gallery system. Entomol.
Exp. Appl. 21, 9–13.
Kingsolver, J.G., Norris, D.M., 1977b. The interaction of Xyleborus ferru-
gineus (Fabr.) (Coleoptera: Scolytidae) behavior and initial repro-
duction in relation to its symbiotic fungi. Ann. Entomol. Soc. Am.
70, 1–4.
Kirejtshuk, A.G., Azar, D., Beaver, R.A., Mandelshtam, M.Y., Nel, A.,
2009. The most ancient bark beetle known: a new tribe, genus and
species from Lebanese amber (Coleoptera, Curculionidae, Scoly-
tinae). Syst. Entomol. 34, 101–112.
Kirisits, T., 2004. Fungal associates of European bark beetles with special
emphasis on the ophiostomatoid fungi. In: Lieutier, F., Keith, R.D.,
Battisti, A., Gre
´goire, J.-C., Evans, H.F. (Eds.), Bark and Wood Boring
Insects in Living Trees in Europe, a Synthesis. Springer, Dordrecht,
pp. 181–237.
Kirkendall, L.R., 1983. The evolution of mating systems in bark and
ambrosia beetles (Coleoptera: Scolytidae and Platypodidae). Zool. J.
Linn. Soc. 77, 293–352.
Kirkendall, L.R., 1984. Notes on the breeding biology of some bigynous
and monogynous Mexican bark beetles (Scolytidae: Scolytus,Thy-
sanoes,Phloeotribus) and records for associated Scolytidae
(Hylocurus,Hypothenemus,Araptus) and Platypodidae (Platypus).
Z. angew. Entomol. 97, 234–244.
Kirkendall, L.R., 1989. Within-harem competition among Ips females, an
overlooked component of density-dependent larval mortality. Hol-
arctic Ecol. 12, 477–487.
Kirkendall, L.R., 1990. Sperm is a limiting resource in the pseudogamous
bark beetle Ips acuminatus (Scolytidae). Oikos 57, 80–87.
Kirkendall, L.R., 1993. Ecology and evolution of biased sex ratios in bark
and ambrosia beetles. In: Wrensch, D.L., Ebbert, M.A. (Eds.), Evo-
lution and Diversity of Sex Ratio in Insects and Mites. Chapman &
Hall, New York, pp. 235–345.
Kirkendall, L., 2006. A new host-specific, Xyleborus vochysiae (Curculio-
nidae: Scolytinae), from Central America breeding in live trees. Ann.
Entomol. Soc. Am. 99, 211–217.
Kirkendall, L., Ødegaard, F., 2007. Ongoing invasions of old-growth
tropical forests: establishment of three incestuous beetle species
in southern Central America (Curculionidae: Scolytinae). Zootaxa.
53–62.
Kirkendall, L.R., Stenseth, N.C., 1990. Ecological and evolutionary sta-
bility of sperm-dependent parthenogenesis: effects of partial
niche overlap between sexual and asexual females. Evolution
44, 698–714.
Kirkendall, L.R., Kent, D.S., Raffa, K.F., 1997. Interactions among
males, females and offspring in bark and ambrosia beetles: the sig-
nificance of living in tunnels for the evolution of social behavior.
In: Choe, J.C., Crespi, B.J. (Eds. ), The Evolution of Social Behavior
in Insects and Arachnids. Cambridge University Press, Cambridge,
pp. 181–215.
Kirkendall, L.R., Faccoli, M., Ye, H., 2008. Description of the Yunnan
shoot borer, Tomicus yunnanensis Kirkendall & Faccoli sp n. (Curcu-
lionidae, Scolytinae), an unusually aggressive pine shoot beetle from
southern China, with a key to the species of Tomicus. Zootaxa
1819, 25–39.
Klein, W.H., Parker, D.L., Jensen, C.E., 1978. Attack, emergence, and
stand depletion trends of mountain pine beetle in a lodgepole pine
stand during an outbreak. Environ. Entomol. 7, 732–737.
Kleine, R., 1931. Die Biologie der Brenthidae. Entomologische Rundschau
48, 149–167, 189–193.
Knee, W., Forbes, M.R., Beaulieu, F., 2013. Diversity and host use of mites
(Acari: Mesostigmata, Oribatida) phoretic on bark beetles (Cole-
optera: Scolytinae): global generalists, local specialists? Ann.
Entomol. Soc. Am. 106, 339–350.
Knı
´z
ˇek, M., 2010. Five new species of Triotemnus (Coleoptera, Curculio-
nidae, Scolytinae) from Morocco and Yemen. ZooKeys 191–206.
Kobayashi, M., Ueda, A., 2002. Preliminary study of mate choice in
Platypus quercivorus (Murayama) (Coleoptera: Platypodidae). Appl.
Entomol. Zool. 37, 451–457.
Koch, R., 1909. Das Larvenleben des Riesenbastka
¨fers Hylesinus (Den-
droctonus) micans. Naturwissenschaftliche Zeitschrift fu
¨r Land- und
Forstwirtschaft 7, 319–340.
Koehler, C.S., Gyrisco, G.G., Newsom, L.D., Schwardt, H.H., 1961.
Biology and control of the clover root borer, Hylastinus obscurus
(Marsham). Memoirs of the Cornell University Agricultural Exper-
iment Station 376, 1–36.
Kolarik, M., Kirkendall, L.R., 2010. Evidence for a new lineage of primary
ambrosia fungi in Geosmithia Pitt (Ascomycota: Hypocreales). Fungal
Biol. 114, 676–689.
Korb, J., Heinze, J., 2008. Ecology of Social Evolution. Springer, Berlin.
Kramer, P., Kozlowsky, T.T., 1979. Physiology of Woody Plants. Aca-
demic Press, New York.
Kramer, A.M., Dennis, B., Liebhold, A.M., Drake, J.M., 2009. The evi-
dence for Allee effects. Popul. Ecol. 51, 341–354.
Ku
¨hnholz, S., Borden, J.H., Uzunovic, A., 2001. Secondary ambrosia
beetles in apparently healthy trees: adaptations, potential causes and
suggested research. Integrated Pest. Manag. Rev. 6, 209–219.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3149
Kuschel, G., 1966. A cossonine genus with bark-beetle habits with remarks
on relationships and biogeography. N. Z. J. Sci. 9, 3–29.
Lachat, T., Nagel, P., Cakpo, Y., Attignon, S., Goergen, G., Sinsin, B.,
Peveling, R., 2006. Dead wood and saproxylic beetle assemblages
in a semi-deciduous forest in southern Benin. Forest Ecol. Manage.
225, 27–38.
Lachat, T., Wermelinger, B., Gossner, M.M., Bussler, H., Isacsson, G.,
Mu
¨ller, J., 2012. Saproxylic beetles as indicator species for dead-wood
amount and temperature in European beech forests. Ecol. Indic.
23, 323–331.
Lake Maner, M., Hanula, J.L., Kristine Braman, S., 2013. Rearing
redbay ambrosia beetle, Xyleborus glabratus (Coleoptera: Curculio-
nidae: Scolytinae), on semi-artificial media. Fla. Entomol.
96, 1042–1051.
Langor, D.W., 1987. Flight muscle changes in the eastern larch beetle,
Dendroctonus simplex LeConte. Coleopterists Bulletin 41, 351–357.
La
˚ngstr€
om, B., 1983. Life cycle and shoot feeding of the pine shoot beetles.
Stud. For. Suec. 163, 1–29.
La
˚ngstr€
om, B., Hellqvist, C., 1993. Induced and spontaneous attacks by
pine shoot beetles on young Scots pine trees—tree mortality and beetle
performance. J. Appl. Entomol. 115, 25–36.
Lanier, G.N., Kirkendall, L.R., 1986. Karyology of pseudogamous Ips bark
beetles. Hereditas 105, 87–96.
Lanier, G.N., Oliver Jr., J.H., 1966. “Sex-ratio” condition: unusual mech-
anisms in bark beetles. Science 150, 208–209.
Latty, T.M., Magrath, M.J.L., Symonds, M.R.E., 2009. Harem size and ovi-
position behaviour in a polygynous bark beetle. Ecol. Entomol.
34, 562–568.
Lawko, C.M., Dyer, E.D.A., 1974. Flight ability of spruce beetles emerging
after attacking frontalin-baited trees. Canada Department of the Envi-
ronment, Canadian Forestry Service, Bi-monthly Research Note
30, 17.
Lekander, B., 1962. Die Borkenka
¨erlarven, ein vernachla
¨ssigter Teil der
Forstentomologie. Dtsch. Entomol. Z. 9, 428–432.
Lekander, B., 1963. Xyleborus cryptographus Ratzb. (Col. Ipidae), Ein
Beitrag zur Kenntnis seiner Verbreitung und Biologie. Entomologisk
Tidskrift 84, 96–109.
Lekander, B., 1968a. Scandinavian bark beetle larvae. Department of
Forest Zoology, Stockholm.
Lekander, B., 1968b. The number of larval instars in some bark beetle
species. Entomologisk Tidskrift 89, 25–34.
Lengerken, H., 1939. Die Brutfu
¨rsorge- und Brutpflegeinstinkte der Ka
¨fer.
Akademische Verlagsgesellschaft m.b.H, Leipzig.
LePelley, R.H., 1968. Pests of Coffee. Longmans, Green and Co., London.
Lewis, E.E., Cane, J.H., 1992. Inefficacy of courtship stridulation as a
premating ethological barrier for Ips bark beetles (Coleoptera: Scoly-
tidae). Ann. Entomol. Soc. Am. 85, 517–524.
Lieutier, F., Ye, H., Yart, A., 2003. Shoot damage by Tomicus sp (Cole-
optera: Scolytidae) and effect on Pinus yunnanensis resistance to sub-
sequent reproductive attacks in the stem. Agr. Forest Entomol.
5, 227–233.
Lieutier, F., Day, K.R., Battisti, A., Gre
´goire, J.-C., Evans, H.F. (Eds.),
2004. Bark and Wood Boring Insects in Living Trees in Europe, a
Synthesis. Kluwer Academic Publishers, Dordrecht.
Lindgren, B.S., Raffa, K.F., 2013. Evolution of tree killing in bark beetles
(Coleoptera: Curculionidae): trade-offs between the maddening
crowds and a sticky situation. Can. Entomol. 145, 471–495.
Linnaeus, C., 1758. Systema Naturae per Regna Tria Naturae: Secundum
Classes, Ordines, Genera, Species, Cum Characteribus, Differentiis,
Synonymis, Locis (10th ed.) (in Latin). Laurentius Salvius, Stockholm.
Lissemore, F.M., 1997. Frass clearing by male pine engraver beetles (Ips
pini; Scolytidae): paternal care or paternity assurance? Behav. Ecol.
8, 318–325.
Lo
´pez, S., Quero, C., Iturrondobeitia, J.C., Guerrero, A., Goldarazena, A.,
2013. Electrophysiological and behavioural responses of Pityophthorus
pubescens (Coleoptera: Scolytinae) to (E, E)-α-farnesene, (R)-(+)-
limonene and (S)-()-verbenone in Pinus radiata (Pinaceae) stands
in northern Spain. Pest Manage. Sci. 69, 40–47.
Lo
´pez-Guille
´n, G., Carrasco, J.V., Cruz-Lo
´pez, L., Barrera, J.F.,
Malo, E.A., Rojas, J.C., 2011. Morphology and structural changes
in flight muscles of Hypothenemus hampei (Coleoptera: Curculio-
nidae) females. Environ. Entomol. 40, 441–448.
L€
ovendal, E.A., 1898. De danske barkbiller (Scolytidæ et Platypodidæ
danicæ) og deres betydning for skov- og havebruget. Det Schu-
botheske Forlag, J.L, Lybecker og E.A. Hirschsprung, Copenhagen.
Løyning, M.K., 2000. Reproductive performance of clonal and sexual bark
beetles (Coleoptera: Scolytidae) in the field. J. Evol. Biol. 13, 743–748.
Løyning, M., Kirkendall, L., 1996. Mate discrimination in a pseudogamous
bark beetle (Coleoptera: Scolytidae): male Ips acuminatus prefer
sexual to clonal females. Oikos 77, 336–344.
Løyning, M.K., Kirkendall, L.R., 1999. Notes on the mating system of
Hylesinus varius (F.) (Col., Scolytidae), a putatively bigynous bark
beetle. J. Appl. Entomol. 123, 77–82.
Lyal, C.H.C., King, T., 1996. Elytro-tergal stridulation in weevils (Insecta:
Coleoptera: Curculionoidea). J. Nat. Hist. 30, 703–773.
Lyons, L.A., 1956. Insects affecting seed production in red pine: Part I
Conophthorus resinosae Hopk. (Coleoptera: Scolytidae). Can.
Entomol. 88, 599–608.
Majka, C.G., Anderson, R.S., McCorquodale, D.B., 2007. The weevils
(Coleoptera: Curculionoidea) of the Maritime Provinces of Canada,
II: New records from Nova Scotia and Prince Edward Island and
regional zoogeography. Can. Entomol. 139, 397–442.
Mandelshtam, M.Y., 2001. New synonymy and new records in Palaearctic
Scolytidae (Coleoptera). Zoosystematica Rossica 9, 203–204.
Maroja, L.S., Bogdanowicz, S.M., Wallin, K.F., Raffa, K.F., Harrison, R.
G., 2007. Phylogeography of spruce beetles (Dendroctonus rufipennis
Kirby) (Curculionidae: Scolytinae) in North America. Mol. Ecol.
16, 2560–2573.
Mattson, W.J., 1980. Cone resources and the ecology of the red pine cone
beetle, Conophthorus resinosae (Coleoptera, Scolytidae). Ann.
Entomol. Soc. Am. 73, 390–396.
McGehey, J.H., 1968. Territorial behaviour of bark-beetle males. Can.
Entomol. 100, 1153.
McKenna, D.D., 2011. Towards a temporal framework for “inordinate
fondness”: Reconstructing the macroevolutionary history of beetles
(Coleoptera). Entomologica Americana 117, 28–36.
McKenna, D.D., Sequeira, A.S., Marvaldi, A.E., Farrell, B.D., 2009. Tem-
poral lags and overlap in the diversification of weevils and flowering
plants. Proc. Natl. Acad. Sci. U. S. A. 106, 7083–7088.
McKnight, M.E., Aarhus, D.G., 1973. Bark beetles, Leperisinus califor-
nicus and L. criddlei (Coleoptera: Scolytidae), attacking green ash
in North Dakota. Ann. Entomol. Soc. Am. 66, 955–957.
McManus, M.L., Giese, R.L., 1968. Columbian timber beetle Corthylus
columbianus. VII. Effect of climatic integrants on historic density fluc-
tuations. For. Sci. 14, 242–253.
McMullen, L.H., Atkins, M.D., 1962. The life history and habits of Sco-
lytus unispinosus Leconte (Coleoptera: Scolytidae) in the interior of
British Columbia. Can. Entomol. 94, 17–25.
McNee, W.R., Wood, D.L., Storer, A.J., 2000. Pre-emergence feeding in
bark beetles (Coleoptera: Scolytidae). Environ. Entomol. 29, 495–501.
150 Bark Beetles
McPherson, J.E., Stehr, F.W., Wilson, L.F., 1970. A comparison between
Conophthorus shoot-infesting beetles and Conophthorus resinosae
(Coleoptera: Scolytidae). 1. Comparative life history studies in
Michigan. Can. Entomol. 102, 1008–1015.
Mecke, R.,Galileo, M.H.M.,2004. A review of the weevilfauna (Coleoptera,
Curculionoidea) of Araucaria angustifolia (Bert.) O. Kuntze (Araucar-
iaceae) in South Brazil. Revista Brasileira de Zoologia 21, 505–513.
Meirmans, S., Skorping, A., Løyning, M.K., Kirkendall, L.R., 2006. On the
track of the Red Queen: bark beetles, their nematodes, local climate
and geographic parthenogenesis. J. Evol. Biol. 19, 1939–1947.
Melnikova, N.I., 1964. Biological significance of the air holes in egg
tunnels of Scolytus ratzeburgi Jans. (Coleoptera, Ipidae). Entomol.
Rev. 43, 16–23.
Menard, K.L., Cognato, A.I., 2007. Mitochondrial haplotypic diversity of
pine cone beetles (Scolytinae: Conophthorus) collected on food
sources. Environ. Entomol. 36, 962–966.
Mendel, Z., 1983. Seasonal history of Orthotomicus erosus (Coleoptera:
Scolytidae) in Israel. Phytoparasitica 11, 13–24.
Merriam, C.H., 1883. Ravages of a rare scolytid beetle in the sugar maples
of northeastern New York. Am. Nat. 17, 84–86.
Meurisse, N., Couillien, D., Gre
´goire, J.-C., 2008. Kairomone traps: a tool
for monitoring the invasive spruce bark beetle Dendroctonus micans
(Coleoptera: Scolytinae) and its specific predator, Rhizophagus
grandis (Coleoptera: Monotomidae). J. Appl. Entomol. 45, 537–548.
Miller, J.M., 1915. Cone beetles: Injury to sugar pine and western yellow
pine. U.S. Department of Agriculture Bulletin 243, 1–12.
Milne, D.H., Giese, R.L., 1969. Biology of the Columbian timber beetle,
Corthylus columbianus (Coleoptera: Scolytidae). IX. Population
biology and gallery characteristics. Entomol. News 80, 225–237.
Milne, D.H., Giese, R.L., 1970. Biology of the Columbian timber beetle,
Corthylus columbianus (Coleoptera: Scolytidae). X. Comparison of
yearly mortality and dispersal losses with population densities.
Entomol. News 81, 12–24.
Mitchell, A., Maddox, C., 2010. Bark beetles (Coleoptera: Curculionidae:
Scolytinae) of importance to the Australian macadamia industry: an
integrative taxonomic approach to species diagnostics. Aust. J.
Entomol. 49, 104–113.
Mitton, J.B., Sturgeon, K.B., 1982. Biotic interactions and evolutionary
change. In: Mitton, J.B., Sturgeon, K.B. (Eds.), Bark Beetles in North
American Conifers. A System for the Study of Evolutionary Biology.
University of Texas Press, Austin, pp. 3–20.
Mizuno, T., Kajimura, H., 2002. Reproduction of the ambrosia beetle,
Xyleborus pfeili (Ratzeburg) (Col., Scolytidae), on semi-artificial diet.
J. Appl. Entomol. 126, 455–462.
Morales-Jime
´nez, J., Vera-Ponce de Leo
´n, A., Garcı
´a-Domı
´nguez, A.,
Martı
´nez-Romero, E., Zu
´n
˜iga, G., Herna
´ndez-Rodrı
´guez, C., 2013.
Nitrogen-fixing and uricolytic bacteria associated with the gut of Den-
droctonus rhizophagus and Dendroctonus valens (Curculionidae: Sco-
lytinae). Microb. Ecol. 66, 200–210.
Morgan, F.D., 1967. Ips grandicollis in South Australia. Aust. For.
31, 137–155.
Morgan, C., 1998. The assessment of potential attractants to beetle pests:
improvements to laboratory pitfall bioassay methods. J. Stored Prod.
Res. 34, 59–74.
Morgan, F.D., Mailu, M., 1976. Behavior and generation dynamics of the
white pine cone beetle Conophthorus coniperda (Schwarz) in central
Wisconsin. Ann. Entomol. Soc. Am. 69, 863–871.
Mueller, U.G., Gerardo, N.M., Aanen, D.K., Six, D.L., Schultz, T.R., 2005.
The evolution of agriculture in insects. Annu. Rev. Ecol. Evol. Syst.
36, 563–595.
Nakashima, T., 1971. Notes on the associated fungi and the mycetangia of
the ambrosia beetle, Crossotarsus niponicus. Appl. Entomol. Zool.
6, 131–137.
Nobuchi, A., 1969. A comparative morphological study of the proven-
triculus in the adult of the superfamily Scolytoidea (Coleoptera). Bull.
Gov. For. Exp. Stn. (Jpn.) 224, 39–110.
Nobuchi, A., 1972. The biology of Japanese Scolytidae and Platypodidae
(Coleoptera). Rev. Plant Prot. Res. 5, 61–75.
Noguera-Martı
´nez, F.A., Atkinson, T.H., 1990. Biogeography and biology
of bark and ambrosia beetles (Coleoptera: Scolytidae and Platypo-
didae) of a mesic montane forest in Mexico, with an annotated
checklist of species. Ann. Entomol. Soc. Am. 83, 453–466.
Nord, J.C., 1972. Biology of the Columbian timber beetle, Corthylus
columbianus (Coleoptera: Scolytidae). Ann. Entomol. Soc. Am.
65, 350–358.
Normark, B.B., 2004. Haplodiploidy as an outcome of coevolution
between male-killing cytoplasmatic elements and their hosts. Evo-
lution 58, 790–798.
Normark, B.B., Kirkendall, L.R., 2009. Parthenogenesis in insects and
mites. In: Resh, V.H., Carde
´, R.T. (Eds.), Encyclopedia of Insects,
Second Edition. Academic Press, Amsterdam, pp. 753–757.
Normark, B.B., Jordal, B.H., Farrell, B.D., 1999. Origin of a haplodiploid
beetle lineage. Proc. R. Soc. B 266, 2253–2259.
Norris, D.M., Chu, H.M., 1980. Symbiote-dependent arrhenotokous par-
thenogenesis in the eukaryote Xyleborus. In: Schwemmler, W.,
Schenk, H.E.A. (Eds.), Endocytobiology: Endosymbiosis and Cell
Biology. Walter de Gruyter & Co., Berlin, pp. 453–460.
Novotny, V., Miller, S.E., Hulcr, J., Drew, R.A.I., Basset, Y., Janda, M.,
et al., 2007. Low beta diversity of herbivorous insects in tropical
forests. Nature 448, 692–698.
Novotny, V., Miller, S.E., Baje, L., Balagawi, S., Basset, Y., Cizek, L.,
et al., 2010. Guild-specific patterns of species richness and host spe-
cialization in plant-herbivore food webs from a tropical forest.
J. Anim. Ecol. 79, 1193–1203.
Nunberg, M., 1963. Zur Systematik und Synonomie der Scolytoidea (Cole-
optera). Ann. Zool. Warszawa 20, 357–361.
Nyland, B.C., 1995. Lowest lifetime fecundity. In: Walker, T.J. (Ed.),
Insect Book of Records. Available online:http://entnemdept.ifas.ufl.
edu/walker/ufbir/chapters/chapter_17.shtml, Last accessed: June 27,
2015.
Ødegaard, F., 2000. The relative importance of trees versus lianas as hosts
for phytophagous beetles (Coleoptera) in tropical forests. J. Biogeogr.
27, 283–296.
Ødegaard, F., 2004. Species richness of phytophagous beetles in the
tropical tree Brosimum utile (Moraceae): the effects of sampling
strategy and the problem of tourists. Ecol. Entomol. 29, 76–88.
Ødegaard, F., 2006. Host specificity, alpha- and beta-diversity of phytoph-
agous beetles in two tropical forests in Panama. Biodiv. Conserv.
15, 83–105.
Ødegaard, F., Diserud, O.H., Engen, S., Aagaard, K., 2000. The magnitude
of local host specificity for phytophagous insects and its implications
for estimates of global species richness. Conserv. Biol. 14, 1182–1186.
Ødegaard, F., Diserud, O.H., Østbye, K., 2005. The importance of plant
relatedness for host utilization among phytophagous insects. Ecol.
Lett. 8, 612–617.
Oester, P.T., Rudinsky, J.A., 1975. Sound production in Scolytidae: strid-
ulation by “silent” Ips bark beetles. Z. angew. Entomol. 79, 421–427.
Oester, P.T., Rudinsky, J.A., 1979. Acoustic behavior of three sympatric
species of Ips (Coleoptera-Scolytidae) co-inhabiting Sitka spruce.
Z. angew. Entomol. 87, 398–412.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3151
Oester, P.T., Rykar, L.C., Rudinsky, J.A., 1978. Complex male premating
stridulation of the bark beetle Hylurgops rugipennis (Mann). Coleop-
terists Bulletin 32, 93–98.
Oester, P.T., Rudinsky, J.A., Ryker, L.C., 1981. Olfactory and acoustic
behavior of Pseudohylesinus nebulosus (Coleoptera, Scolytidae) on
Douglas-fir bark. Can. Entomol. 113, 645–650.
Ohmart, C.P., 1989. Why are there so few tree-killing bark beetles asso-
ciated with angiosperms? Oikos 54, 242–245.
Ohya, E., Kinuura, H., 2001. Close range sound communications of the oak
platypodid beetle Platypus quercivorus (Murayama) (Coleoptera: Pla-
typodidae). Appl. Entomol. Zool. 36, 317–321.
Okello, S., Reichmuth, C., Schulz, F.A., 1996a. Observations on the
biology and host specificity of Pagiocerus frontalis (Fabricius) (Cole-
optera: Scolytidae) at 20 C and 25 C and 75% rh. Zeitschrift fu
¨r
Pflanzenkrankheiten und Pflanzenschutz 103, 377–382.
Okello, S.,Reichmuth, C., Schulz,F.A., 1996b. Laboratory investigations on
the developmental rate at low relative humidity and the developmental
temperature limit of Pagiocerus frontalis (Fab) (Col, Scolytidae) at high
and low temperatures. Anz. Scha
¨dlingskd. 69, 180–182.
Page, R.E., Willis, M.A., 1983. Sexual dimorphism in ventral abdominal
setae in Scolytus multistriatus (Coleoptera: Scolytidae): possible role
in courtship behavior. Ann. Entomol. Soc. Am. 76, 78–82.
Page, M., Nelson, L.J., Haverty, M.I., Blomquist, G.J., 1990a. Cuticular
hydrocarbons as chemotaxonomic characters for bark beetles: Den-
droctonus ponderosae,D. jeffreyi,D. brevicomis, and D. frontalis
(Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 83, 892–902.
Page, M., Nelson, L.J., Haverty, M.I., Blomquist, G.J., 1990b. Cuticular
hydrocarbons of eight species of North American cone beetles, Con-
ophthorus Hopkins. J. Chem. Ecol. 16, 1173–1198.
Page, M., Nelson, L.J., Blomquist, G.J., Seybold, S.J., 1997. Cuticular
hydrocarbons as chemotaxonomic characters of pine engraver beetles
(Ips spp.) in the grandicollis subgeneric group. J. Chem. Ecol.
23, 1053–1099.
Paine, T.D. (Ed.), 2006. Invasive Forest Insects, Introduced Forest Trees,
and Altered Ecosystems. Springer, Dordrecht.
Paine, T.D., Raffa, K.F., Harrington, T.C., 1997. Interactions among sco-
lytid bark beetles, their associated fungi, and live conifers. Annu. Rev.
Entomol. 42, 179–206.
Peer, K., Taborsky, M., 2005. Outbreeding depression, but no inbreeding
depression in haplodiploid ambrosia beetles with regular sibling
mating. Evolution 59, 317–323.
Peer, K., Taborsky, M., 2007. Delayed dispersal as a potential route to
cooperative breeding in ambrosia beetles. Behav. Ecol. Sociobiol.
61, 729–739.
Peleg, B., Norris, D.M., 1973. Oocyte activation in Xyleborus ferrugineus
by bacterial symbionts. J. Insect Physiol. 19, 137–145.
Petty, J.L., 1977. Bionomics of two aspen bark beetles, Trypophloeus
populi and Procryphalus mucronatus (Coleoptera: Scolytidae).
Western Great Basin Nat. 37, 105–127.
Pfeffer, A., 1955. Fauna CSR, Kurovci—Scolytoidea. Nakaldatelstvı
´
CSAV, Praha.
Pfeffer, A., 1995. Zentral- und westpala
¨arktische Borken- und Kernka
¨fer
(Coleoptera: Scolytidae, Platypodidae). Entomologica Brasiliensia
17, 5–310.
Ploetz, R.C., Hulcr, J., Wingfield, M.J., de Beer, Z.W., 2013. Destructive
tree diseases that are associated with ambrosia and bark beetles: black
swan events in tree pathology? Plant Dis. 97, 856–872.
Pope, D.N., Coulson, R.N., Fargo, W.S., Gagne, J.A., Kelly, C.W., 1980.
The allocation process and between-tree survival probabilities in Den-
droctonus frontalis infestations. Res. Popul. Ecol. 22, 197–210.
Postner, M., 1974. Scolytidae (¼Ipidae), Borkenka
¨fer. In: Schwenke, W.
(Ed.), Die Forstscha
¨dlinge Europas. Bind 2, Ka
¨fer. Paul Parey,
Hamburg, pp. 334–482.
Pureswaran, D.S., Borden, J.H., 2003. Is bigger better? Size and
pheromone production in the mountain pine beetle, Dendroctonus
ponderosae Hopkins (Coleoptera: Scolytidae). J. Insect Behav. 16,
765–782.
Queller, D.C., Strassmann, J.E., 1998. Kin selection and social insects. Bio-
Science 48, 165–175.
Rabinowitz, D., 1977. Effects of a mangrove borer, Poecilips rhizophorae,
on propagules of Rhizophora harrisonii in Panama
´.Fla. Entomol.
60, 129–134.
Raffa, K.F., Aukema, B.H., Bentz, B.J., Carroll, A.L., Hicke, J.A.,
Turner, M.G., Romme, W.H., 2008. Cross-scale drivers of natural dis-
turbances prone to anthropogenic amplification: the dynamics of bark
beetle eruptions. BioScience 58, 501–517.
Rappaport, N.G., Stein, J.D., del Rio Mora, A.A., Debarr, G.L., De
Groot, P., Mori, S., 2000. Cone beetle (Conophthorus spp.) (Cole-
optera: Scolytidae) responses to behavioral chemicals in field trials:
a transcontinental perspective. Can. Entomol. 132, 925–937.
Ratzeburg, J.T.C., 1839. Die Forst-Insecten. Nicolaische Buchhandlung,
Berlin.
Reid, R.W., 1958. Internal changes in the female mountain pine beetle,
Dendroctonus monticolae Hopk., associated with egg laying and
flight. Can. Entomol. 90, 464–468.
Reid, M.L., 1999. Monogamy in the bark beetle Ips latidens: ecological
correlates of an unusual mating system. Ecol. Entomol. 24, 89–94.
Reid, M.L., Robb, T., 1999. Death of vigorous trees benefits bark beetles.
Oecologia 120, 555–562.
Reid, M.L., Roitberg, B.D., 1994. Benefits of prolonged male residence
with mates and brood in pine engravers (Coleoptera, Scolytidae).
Oikos 70, 140–148.
Reid, M.L., Roitberg, B.D., 1995. Effects of body-size on investment
in individual broods by male pine engravers Can. J. Zool. 73,
1396–1401.
Reitter, E., 1916. Fauna Germanica. V Band. Die Ka
¨fer des Deutschen
Reiches, K. G. Lutz, Stuttgard.
Rexrode, C.O., 1982. Bionomics of the peach bark beetle Phloeotribus
liminaris (Coleoptera: Scolytidae) in black cherry. J. Georgia
Entomol. Soc. 17, 388–398.
Roberts, H., 1960. Trachyostus ghanaensis Schedl (Col., Platypodidae) an
ambrosia beetle attacking Wawa, Triplochiton scleroxylon K. Schum.
West Afr. Timber Borer Res. Unit Tech. Bull. No. 3, 1–17.
Roberts, H., 1962. A description of the developmental stages of Tra-
chyostus aterrimus a West African Platypodina, and some remarks
on its biology. Fifth Report West African Timber Borer Research Unit
1961–62, 29–46.
Roberts, H., 1968. Notes on biology of ambrosia beetles of genus Tra-
chyostus Schedl (Coleoptera—Platypodidae) in West Africa. Bull.
Entomol. Res. 58, 325–352.
Roberts, H., 1969. Forest insects of Nigeria with notes on their biology and
distribution. Commonwealth Forestry Institute Paper 44, 1–206.
Roberts, H., 1976. Observations on the biology of some tropical rain forest
Scolytidae (Coleoptera) from Fiji I. Subfamilies—Hylesininae, Ipinae
(excluding Xyleborini). Bull. Entomol. Res. 66, 373–388.
Robertson, I.C., 1998a. Flight muscle changes in male pine engraver
beetles during reproduction: the effects of body size, mating status
and breeding failure. Physiol. Entomol. 23, 75–80.
Robertson, I.C., 1998b. Paternal care enhances male reproductive success
in pine engraver beetles. Anim. Behav. 56, 595–602.
152 Bark Beetles
Robertson, I.C., 2000. Reproduction and developmental phenology of Ips
perturbatus (Coleoptera: Scolytidae) inhabiting white spruce
(Pinaceae). Can. Entomol. 132, 529–537.
Robertson, I.C., Roitberg, B.D., 1998. Duration of paternal care in pine
engraver beetles: why do larger males care less? Behav. Ecol.
Sociobiol. 43, 379–386.
Roeper, R.A., 1995. Patterns of mycetophagy in Michigan ambrosia
beetles. Michigan Academian 27, 153–161.
Roeper, R.A., Treeful, L.M., Foote, R.A., Bunce, M.A., 1980a. In vitro
culture of the ambrosia beetle Xyleborus affinis (Coleoptera: Scoly-
tidae). Great Lakes Entomologist 13, 33–35.
Roeper, R., Treeful, L.M., O’Brien, K.M., Foote,R.A., Bunce, M.A., 1980b.
Life history of the ambrosia beetle Xyleborus affinis (Coleoptera:
Scolytidae) from in vitro culture.Great Lakes Entomologist 13, 141–144.
Roeper, R.A., Zestos, D.V., Palik, B.J., Kirkendall, L.R., 1987a.
Distribution and host plants of Corthylus punctatissimus (Coleoptera:
Scolytidae) in the lower peninsula of Michigan. Great Lakes Entomol-
ogist 20, 69–70.
Roeper, R.A., Palik, B.J., Zestos, D.V., Hesch, P.G., Larsen, C.D., 1987b.
Observations of the habits of Corthylus punctatissimus (Coleoptera,
Scolytidae) infesting maple saplings in Central Michigan. Great Lakes
Entomologist 20, 173–176.
Rohlfs, M., 2005. Density-dependent insect–mold interactions:
effects on fungal growth and spore production. Mycologia 97,
996–1001.
Rohlfs, M., Churchill, A.C.L., 2011. Fungal secondary metabolites as mod-
ulators of interactions with insects and other arthropods. Fungal Genet.
Biol. 48, 23–34.
Ruckes Jr., H., 1963. Cone beetles of the genus Conophthorus in California
(Coleoptera: Scolytidae). Pan-Pac. Entomol. 39, 43–50.
Rudinsky, J.A., 1969. Masking of the aggregating pheromone in Dendroc-
tonus pseudotsugae Hopk. Science 166, 884–885.
Rudinsky, J.A., 1976. Various host–insect interrelations in host-finding
and colonization behavior of bark beetles on coniferous trees. Symp.
Biol. Hung. 16, 229–235.
Rudinsky, J.A., 1979. Chemoacoustically induced behavior of Ips typo-
graphus (Col, Scolytidae). Z. angew. Entomol. 88, 537–541.
Rudinsky, J.A., Michael, R.R., 1974. Sound production in Scolytidae:
“rivalry” behaviour of male Dendroctonus beetles. J. Insect Physiol.
20, 1219–1230.
Rudinsky, J.A., Ryker, L.C., 1976. Sound production in Scolytidae—
rivalry and premating stridulation of male Douglas-fir beetle. J. Insect
Physiol. 22, 997–999.
Rudinsky, J.A., Vallo, V., 1979. The ash bark beetles Leperisinus fraxini
and Hylesinus oleiperda: stridulatory organs, acoustic signals, and
pheromone production. Z. angew. Entomol. 87, 417–429.
Rudinsky, J.A., Ryker, L.C., Michael, R.R., Libbey, L.M., Morgan, M.E.,
1976. Sound production in Scolytidae: female sonic stimulus of male
pheromone release in two Dendroctonus beetles. J. Insect Physiol.
22, 1675–1681.
Rudinsky, J.A., Vallo, V., Ryker, L.C., 1978. Sound production in Scoly-
tidae: attraction and stridulation of Scolytus mali (Col., Scolytidae).
Z. angew. Entomol. 86, 381–391.
Ru
¨hm, W., 1981. Zur Biologie und €
Okologie von Pteleobius (Xylechinus)
valdivianus (Eggers, 1942) (Col., Scolytidae), einer vorwiegend an
untersta
¨ndigen Araukarien, Araucaria araucana (Mol.) Koch, bru
¨-
tenden Borkenka
¨ferart. Entomologische Mitteilungen aus dem Zoolo-
gischen Museum Hamburg 7, 13–20.
Ryker, L.C., 1984. Acoustic and chemical signals in the life cycle of a
beetle. Sci. Am. 250, 112–123.
Safranyik, L., 1976. Size- and sex-related emergence, and survival in
cold storage, of mountain pine beetle adults. Can. Entomol.
108, 209–212.
Salom, S.M., McLean, J.A., 1989. Influence of wind on the spring flight of
Trypodendron lineatum (Olivier) (Coleoptera, Scolytidae) in a second-
growth coniferous forest. Can. Entomol. 121, 109–119.
Salom, S.M., McLean, J.A., 1991. Environmental influences on dispersal
of Trypodendron lineatum (Coleoptera, Scolytidae). Environ.
Entomol. 20, 565–576.
Salonen, K., 1973. On the life cycle, especially on the reproduction biology
of Blastophagus piniperda L. (Col., Scolytidae). Acta For. Fenn.
127, 1–72.
Santoro, F.H., 1963. Bioecologı
´adePlatypus sulcatus Chapuis (Coe-
loptera, Platypodidae). Revista de Investigaciones Forestales 4, 47–79.
Santos, M.F., de, A., Mermudes, J.R.M., da Fonseca, V.M.M., 2011. A
specimen of Curculioninae (Curculionidae, Coleoptera) from the
Lower Cretaceous, Araripe Basin, north-eastern Brazil. Palaeontology
54, 807–814.
Sasakawa, M., Yoshiyasu, Y., 1983. Stridulatory organs of the Japanese
pine bark beetles (Coleoptera, Scolytidae). Kontyu 51, 493–501.
Saunders, J.L., Knoke, J.K., 1967. Diets for rearing the ambrosia beetle
Xyleborus ferrugineus (Fabricius) in vitro. Science 157, 460–463.
Sauvard, D., 2004. General biology of bark beetles. In: Lieutier, F.,
Day, K.R., Battisti, A., Gre
´goire, J.-C., Evans, H.F. (Eds.), Bark
and Wood Boring Insects in Living Trees in Europe, A Synthesis.
Kluwer Academic Publishers, Dordrecht, pp. 63–88.
Schedl, K.E., 1931. Morphology of the bark beetles of the genus Gnatho-
trichus Eichhoff. Smithson. Misc. Collect. 82, 1–88.
Schedl, K.E., 1958. Breeding habits of arboricole insects in Central Africa.
Tenth International Congress of Entomology, Proceedings,183–197.
Schedl, K.E., 1959. Scolytidae und Platypodidae Afrikas. Band 1. Familie
Scolytidae. Revista de Entomologia de Moc¸ambique 2, 357–422.
Schedl, K.E., 1960a. Scolytidae und Platypodidae Afrikas. Band 1 (forts.).
Familie Scolytidae. Revista de Entomologia de Moc¸ambique
3, 75–154.
Schedl, K.E., 1960b. Insectes nuisibles aux fruits et aux graines. Publica-
tions de l’Institut National pour l’e
´tude agronomique du Congo Belge,
Se
´rie Scientifique 82, 1–133.
Schedl, K.E., 1961. Scolytidae und Platypodidae Afrikas. Band 1 (forts.).
Familie Scolytidae. Revista de Entomologia de Moc¸ambique
4, 335–742.
Schedl, K.E., 1962a. Scolytidae und Platypodidae Afrikas. Band 2. Familie
Scolytidae. Revista de Entomologia de Moc¸ambique 5, 1–594.
Schedl, K.E., 1962b. Scolytidae und Platypodidae Afrikas. Band 3. Familie
Platypodidae. Revue Entomologique de Moc¸ ambique 5, 595–1352.
Schedl, K.E., 1972. Monographie der Familie Platypodidae Coleoptera.
W. Junk, Den Haag.
Schedl, K.E., 1974. Scolytoidea from the Galapagos and Cocos Islands.
Studies of the Neotropical Fauna 9, 47–53.
Schedl, K.E., 1977. Die Scolytidae und Platypodidae Madagaskars und
einiger naheliengender Inselgruppen. 303 Bietrag. Mitt. Forstl.
Bundes-Versuchanstalt, Wien 119, 5–326.
Schlupp, I., 2005. The evolutionary ecology of gynogenesis. Annu. Rev.
Ecol. Evol. Syst. 36, 399–417.
Schlyter, F., Zhang, Q.-H., 1996. Testing avian polygyny hypotheses in
insects: harem size distribution and female egg gallery spacing in three
Ips bark beetles. Oikos 76, 57–69.
Schmidberger, J., 1836. Naturgeschichte des Apfelborkenka
¨fers Apate
dispar. Beitra
¨ge zur Obstbaumzucht und zur Naturgeschichte der
den Obstba
¨umen scha
¨dlichen Insekten 4, 213–230.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3153
Schneider, I., 1987. Distribution, fungus-transfer and gallery construction
of the ambrosia beetle Xyleborus affinis in comparison with
X. mascarensis (Coleoptera, Scolytidae). Entomologia Generalis
12, 267–275.
Schneider-Orelli, O., 1911. Die Uebertragung und Keimung des Ambrosia-
pilzes von Xyleborus (Anisandrus) dispar F. Naturwissenschaftliche
Zeitschrift fu
¨r Land- und Forstwirtschaft 8, 186–192.
Schrey, N.M., Schrey, A.W., Heist, E.J., Reeve, J.D., 2011. Genetic hetero-
geneity in a cyclical forest pest, the southern pine beetle, Dendroc-
tonus frontalis, is differentiated into east and west groups in the
southeastern United States. J. Insect Sci. 11, 110.
Schwarz, E.A., 1891. Notes on the breeding habits of some scolytids. Proc.
Entomol. Soc. Wash. 2, 77–80.
Schwarz, E.A., 1901. Note on Scolytus quadrispinosus. Proc. Entomol.
Soc. Wash. 4, 344.
Scott, J.J., Oh, D.C., Yuceer, M.C., Klepzig, K.D., Clardy, J., Currie, C.R.,
2008. Bacterial protection of beetle-fungus mutualism. Science
322, 63.
Searcy, W.A., Yasukawa, K., 1989. Alternative models of territorial
polygyny in birds. Am. Nat. 134, 323–343.
Sforzi, A., Bartolozzi, L., 2004. Brenthidae of the World. Museo Regionale
di Scienze Naturali. Torino, Italy.
Shimizu, A., Tanaka, R., Akiba, M., Masuya, H., Iwata, R., Fukuda, K.,
Kanzaki, N., 2013. Nematodes associated with Dryocoetes uniseriatus
(Coleoptera: Scolytidae). Environ. Entomol. 42, 79–88.
Shuster, S.M., Wade, M.J., 2003. Mating Systems and Strategies. Princeton
University Press, Princeton and Oxford.
Singer, T., 1998. Roles of hydrocarbons in the recognition systems of
insects. Am. Zool. 38, 394–405.
Six, D.L., 2003. Bark beetle-fungus symbioses. In: Bourtzis, K., Miller, T.A.
(Eds.), Insect Symbiosis. CRC Press, Boca Raton, pp. 97–114.
Six, D.L., 2012. Ecological and evolutionary determinants of bark beetle–
fungus symbioses. Insects 3, 339–366.
Six, D., 2013. The bark beetle holobiont: Why microbes matter. J. Chem.
Ecol. 1–14.
Six, D.L., Paine, T.D., 1998. Effects of mycangial fungi and host tree
species on progeny survival and emergence of Dendroctonus
ponderosae (Coleoptera: Scolytidae). Environ. Entomol. 27,
1393–1401.
Smetanin, A.N., 2013. A new bark beetle species, Dryocoetes krivolutz-
kajae Mandelshtam, 2001 (Scolytidae), discovered in Kamchatka.
Contemp. Probl. Ecol. 6, 43–44.
Smith, N.G.C., 2000. The evolution of haplodiploidy under inbreeding.
Heredity 84, 186–192.
Smith, S.M., Cognato, A.I., 2010. A taxonomic revision of Camptocerus
Dejean (Coleoptera: Curculionidae: Scolytinae). Insecta Mundi
148, 1–88.
Smith, S.M., Cognato, A.I., 2011. Observations of the biology of Campto-
cerus Dejean (Coleoptera: Curculionidae: Scolytinae) in Peru. Coleop-
terists Bulletin 65, 27–32.
Smith, G.D.,Carroll, A.L., Lindgren, B.S., 2009. Life history of a secondary
bark beetle, Pseudips mexicanus (Coleoptera: Curculionidae:
Scolytinae), in lodgepole pine in British Columbia. Can. Entomol.
141, 56–69.
Sousa, W.P., Quek, S.P., Mitchell, B.J., 2003. Regeneration of Rhizophora
mangle in a Caribbean mangrove forest: interacting effects of canopy
disturbance and a stem-boring beetle. Oecologia 137, 436–445.
Speight, M.R., Wainhouse, D., 1989. Ecology and Management of Forest
Insects. Clarendon Press, Oxford.
Stacey, P.B., Ligon, J.D., 1991. The benefits-of-philopatry hypothesis for
the evolution of cooperative breeding variation in territory quality and
group-size effects. Am. Nat. 137, 831–846.
Stahlhut, J.K., Desjardins, C.A., Clark, M.E., Baldo, L., Russell, J.A.,
Werren, J.H., Jaenike, J., 2010. The mushroom habitat as an ecological
arena for global exchange of Wolbachia. Mol. Ecol. 19, 1940–1952.
Stark, R.W., 1982. Generalized ecology and life cycle of bark beetles.
In: Mitton, J.B., Sturgeon, K.B. (Eds.), Bark Beetles in North
American Conifers. A System for the Study of Evolutionary Biology.
University of Texas Press, Austin, pp. 21–45.
Stauffer, C., van Meer, M.M.M., Riegler, M., 1997. The presence of the
protobacteria Wolbachia in European Ips typographus (Col, Scoly-
tidae) populations and the consequences for genetic data. Mitteilungen
der Deutschen Gesellschaft fu
¨r allgemeine und angewandte Entomo-
logie 11, 709–711.
Stilwell, A.R., Smith, S.M., Cognato, A.I., Martinez, M., Flowers, R.W.,
2014. Coptoborus ochromactonus, n. sp. (Coleoptera: Curculionidae:
Scolytinae), an emerging pest of cultivated balsa (Malvales:
Malvaceae) in Ecuador. J. Econ. Entomol. 107, 675–683.
Stone, C., 1990. Parasitic and phoretic nematodes associated with Ips
grandicollis (Coleoptera, Scolytidae) in New-South-Wales. Nemato-
logica 36, 478–480.
Storer, A.J., Wainhouse, D., Speight, M.R., 1997. The effect of larval
aggregation behaviour on larval growth of the spruce bark beetle Den-
droctonus micans. Ecol. Entomol. 22, 109–115.
Strohmeyer, H., 1906. Neue Untersuchungen u
¨ber Biologie, Scha
¨dlichkeit
und Vorkommen des Eichenkernka
¨fers, Platypus cylindrus var.
cylindriformis. Naturwissenschaftliche Zeitschrift fur Land- und
Forstwirtschaft 4, 329–341, 408–421, 506–511.
Strohmeyer, H., 1918. Die Morphologic des Chitinskeletts der Platypo-
diden. Archiv fuer Naturgeschichte Berlin Abt A 84, 1–42.
Sullivan, B.T., Nin
˜o, A., Moreno, B., Brownie, C., Macı
´as-Sa
´mano, J.,
Clarke, S.R., et al., 2012. Biochemical evidence that Dendroctonus
frontalis consists of two sibling species in Belize and Chiapas. Mexico.
Ann. Entomol. Soc. Am. 105, 817–831.
Sun, J.H., Lu, M., Gillette, N.E., Wingfield, M.J., 2013. Red turpentine
beetle: innocuous native becomes invasive tree killer in China. Annu.
Rev. Entomol. 58, 293–311.
Susoy, V., Herrmann, M., 2014. Preferential host switching and codiver-
gence shaped radiation of bark beetle symbionts, nematodes of Mico-
letzkya (Nematoda: Diplogastridae). J. Evol. Biol. 27, 889–898.
Swaby, J.A., Rudinsky, J.A., 1976. Acoustic and olfactory behaviour of Ips
pini (Say) (Coleoptera: Scolytidae) during host invasion and coloni-
sation. Z. angew. Entomol. 81, 421–432.
Swaine, J.M., 1918. Canadian bark-beetles, part II. A preliminary classifi-
cation, with an account of the habits and means of control. Canadian
Department of Agriculture, Division of Entomology, Bulletin
14, 1–143.
Swedenborg, P.D., Jones, R.L., Ascerno, M.E., Landwehr, V.R., 1988.
Hylurgopinus rufipes (Eichhoff) (Coleoptera: Scolytidae): attraction
to broodwood, host colonization behavior, and seasonal activity in
central Minnesota. Can. Entomol. 120, 1041–1050.
Swedenborg, P.D., Jones, R.L., Ryker, L.C., 1989. Stridulation and
associated behavior of the native elm bark beetle Hylurgopinus
rufipes (Eichhoff) (Coleoptera: Scolytidae). Can. Entomol.
121, 245–252.
Swift, M.J., 1977. The roles of fungi and animals in the immobilization and
release of nutrient elements from decomposing branchwood. Ecol.
Bull. 25, 193–202.
154 Bark Beetles
Tallamy, D.W., 1994. Nourishment and the evolution of paternal
investment in subsocial arthropods. In: Hunt, J.H., Nalepa, C.A.
(Eds.), Nourishment and Evolution in Insect Societies. Westview
Press, Boulder, pp. 21–55.
Tallamy, D.W., Wood, R.F., 1986. Convergence patterns in subsocial
insects. Annu. Rev. Entomol. 31, 369–390.
Thompson, R.T., 1996. The species of Phaenomerus Sch€
onherr (Cole-
optera: Curculionidae: Zygopinae) of the Australian region. Inverte-
brate Taxonomy 10, 937–993.
Thornhill, N.W., 1993. The Natural History of Inbreeding and Out-
breeding: Theoretical and Empirical Perspectives. University of
Chicago Press, Chicago.
Ticheler, J.H.G., 1961. An analytical study of the epidemiology of the
coffee berry borer in the Ivory Coast. Mededelingen van de Landbou-
whogeschool te Wageningen 61 (11), 1–49, 1–13.
Tra
¨ga
˚rdh, I., 1930. Studies on the galleries of bark beetles. Bull. Entomol.
Res. 21, 469–480.
Tredl, R., 1915. Aus dem Leben des Birkensplintka
¨fers, Scolytus ratze-
burgi. Entomologische Bla
¨tter 11, 146–154.
Trimble, F.M., 1924. Life history and habits of two Pacific coast bark
beetles. Ann. Entomol. Soc. Am. 17, 382–391.
Tykarski, P., 2006. Beetles associated with scolytids (Coleoptera, Scoly-
tidae) and the elevational gradient: diversity and dynamics of the com-
munity in the Tatra National Park. Poland. Forest Ecol. Manage.
225, 146–159.
Ulyshen, M.D., Hanula, J.L., Horn, S., Kilgo, J.C., Moorman, C.E., 2004.
Spatial and temporal patterns of beetles associated with coarse woody
debris in managed bottomland hardwood forests. Forest Ecol. Manage.
199, 259–272.
Vega, F.E., Benavides, P., Stuart, J.A., O’Neill, S.L., 2002. Wolbachia
infection in the coffee berry borer (Coleoptera: Scolytidae). Ann.
Entomol. Soc. Am. 95, 374–378.
Vega, F.E., Davis, A.P., Jaramillo, J., 2012. From forest to plantation?
Obscure articles reveal alternative host plants for the coffee berry
borer, Hypothenemus hampei (Coleoptera: Curculionidae). Biol. J.
Linn. Soc. 107, 86–94.
Vega, F.E., Simpkins, A., Bauchan,G., Infante, F., Kramer, M., Land, M.F.,
2014. On the eyes of male coffee berry borers as rudimentary organs.
PLoS One 9 (1), e85860.
Vernoff, S., Rudinsky, J.A., 1980. Sound production and pairing behavior
of Leperisinus californicus Swaine and L. oreganus Blackman (Cole-
optera: Scolytidae) attacking Oregon ash. Z. angew. Entomol.
90, 58–74.
Wallace, A.R., 1860. Notes on the habits of Scolytidae and Bostrichidae.
Transactions of the Entomological Society of London (n. s.) 5 (Part
IV), 218–220.
Wang, C.S., 1981. A study of the Korean pine bark beetle (Blastophagus
pilifer Spess). Kunchong Zhishi [Insect Knowledge] 18, 165–167
[in Chinese, with English abstract].
Weber, B.C., McPherson, J.E., 1983. Life history of the ambrosia beetle
Xylosandrus germanus (Coleoptera: Scolytidae). Ann. Entomol.
Soc. Am. 76, 455–462.
Webster, F.M., 1910. The clover root-borer (Hylastinus obscurus
Marsham.). U.S. Department of Agriculture, Bureau of Entomology
Circular no 119, 1–5.
Werren, J.H., Baldo, L., Clark, M.E., 2008. Wolbachia: master manipu-
lators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751.
West, S.A., Pen, I., Griffin, A.S., 2002. Cooperation and competition
between relatives. Science 296, 72–75.
White, T.C.R., 1993. The Inadequate Environment. Nitrogen and the
Abundance of Animals. Springer-Verlag, Berlin.
Wichmann, H.E., 1927. Ipidae. In: Schulze, P. (Ed.), Biologie der Tiere
Deutschlands. Gebru
¨der Borntra
¨ger, Berlin, pp. 347–381.
Wichmann, H.E., 1967. Die Wirkungsbreite des Ausstoßreflexes bei Bor-
kenka
¨fern. J. Pest Sci. 40, 184–187.
Wilson, H.F., 1909. The peach-tree barkbeetle. U.S. Department of Agri-
culture, Bureau of Entomology, Bulletin 68, 91–108.
Wilson, E.O., 1971. The Insect Societies. Belknap Press of Harvard Uni-
versity, Cambridge.
Wilson, E.O., 1975. Sociobiology: The New Synthesis. Harvard University
Press, Cambridge.
Wilson, E.O., H€
olldobler, B., 1980. Sex-differences in cooperative silk-
spinning by weaver ant larvae. Proc. Natl. Acad. Sci. U. S. A.
77, 2343–2347.
Wilson-Rich, N., Spivak, M., Fefferman, N.H., Starks, P.T., 2009. Genetic,
individual, and group facilitation of disease resistance in insect soci-
eties. Annu. Rev. Entomol. 54, 405–423.
Wood, S.L., 1978. A reclassification of the subfamilies and tribes of Sco-
lytidae (Coleoptera). Annales de la Socie
´te
´entomologique de France
(Neauveau Series) 14, 95–122.
Wood, D.L., 1982. The role of pheromones, kairomones, and allomones in
the host selection and colonization behavior of bark beetles. Annu.
Rev. Entomol. 27, 411–446.
Wood, S.L., 1982. The bark and ambrosia beetles of North and Central
America (Coleoptera: Scolytidae), a taxonomic monograph. Great
Basin Nat. Mem. 6, 1–1359.
Wood, S.L., 1983. Scolytodes atratus panamensis (Escarbajito de guarumo,
Cecropia petiole borer). In: Janzen, D.H. (Ed.), Costa Rican Natural
History. University of Chicago Press, Chicago, pp. 768–769.
Wood, S.L., 1986. A reclassification of the genera of Scolytidae (Cole-
optera). Great Basin Nat. Mem. 10, 1–126.
Wood, S.L., 1993. Revision of the genera of Platypodidae (Coleoptera).
Great Basin Nat. 53, 259–281.
Wood, S.L., 2007. Bark and Ambrosia Beetles of South America (Cole-
optera, Scolytidae). Brigham Young University, Provo.
Wood, S.L., Bright, D.E., 1987. A catalog of Scolytidae and Platypodidae
(Coleoptera), Part 1: Bibliography. Great Basin Nat. Mem. 11, 1–685.
Wood, S.L., Bright Jr., D.E., 1992. A catalog of Scolytidae and Platypo-
didae (Coleoptera), Part 2: Taxonomic Index. Volumes A and B. Great
Basin Nat. Mem. 13, 1–1553.
Yan, Z.L., Sun, J.H., Don, O., Zhang, Z.N., 2005. The red turpentine beetle,
Dendroctonus valens LeConte (Scolytidae): an exotic invasive pest of
pine in China. Biodivers. Conserv. 14, 1735–1760.
Ye, H., 1997. Mass attack by Tomicus piniperda L. (Col., Scolytidae)
on Pinus yunnanensis tree in the Kunming region, southwest China.
In: Gre
´goire, J.-C., Liebhold, A.M., Stephen, F.M., Day, K.R.,
Salom, S.M. (Eds.), Proceedings: Integrating Cultural Tactics into
the Management of Bark Beetle and Reforestation Pests,
pp. 225–227, USDA Forest Service General Technical Report NE-236.
Ye, H., Ding, X.S., 1999. Impacts of Tomicus minor on distribution
and reproduction of Tomicus piniperda (Col., Scolytidae) on the
trunk of the living Pinus yunnanensis trees. J. Appl. Entomol.
123, 329–333.
Yearian, W.C., Gouger, R.J., Wilkinson, R.C., 1972. Effects of the blue-
stain fungus, Ceratocystis ips, on development of Ips bark beetles in
pine bolts. Ann. Entomol. Soc. Am. 65, 481–487.
Ytsma, G., 1988. Stridulation in Platypus apicalis,P. caviceps, and
P. gracilis (Col., Platypodidae). J. Appl. Entomol. 11, 256–261.
Evolution and Diversity of Bark and Ambrosia Beetles Chapter 3155
Yust, H.R., 1957. Biology and habits of Pagiocerus fiorii in Ecuador.
J. Econ. Entomol. 50, 92–96.
Zanuncio, A.J.V., Pastori, P.L., Kirkendall, L.R., Lino-Neto, J., Serra
˜o, J.E.,
Zanuncio, J.C., 2010. Megaplatypus mutatus (Chapuis) (Coleoptera:
Curculionidae: Platypodinae) attacking hybrid Eucalyptus clones in
southern Espirito Santo, Brazil. Coleopterists Bulletin 61, 81–83.
Zanzot, J.W., Matusick, G., Eckhardt, L.G., 2010. Ecology of root-feeding
beetles and their associated fungi on longleaf pine in Georgia. Environ.
Entomol. 39, 415–423.
Zchori-Fein, E., Borad, C., Harari, A.R., 2006. Oogenesis in the date stone
beetle, Coccotrypes dactyliperda, depends on symbiotic bacteria.
Physiol. Entomol. 31, 164–169.
Zhang, L.L., Chen, H., Ma, C., Tian, Z.G., 2010. Electrophysiological
responses of Dendroctonus armandi (Coleoptera: Curculionidae:
Scolytinae) to volatiles of Chinese white pine as well as to pure enan-
tiomers and racemates of some monoterpenes. Chemoecology
20, 265–275.
Zrimec, M.B., Zrimec, A., Slanc, P., Kac, J., Kreft, S., 2004. Screening
for antibacterial activity in 72 species of wood-colonizing fungi by
the Vibrio fisheri bioluminescence method. J. Basic Microbiol.
44, 407–412.
Zu
´n
˜iga, G., Cisneros, R., Hayes, J.L., Macias-Samano, J., 2002a. Karyology,
geographic distribution, and origin of the genus Dendroctonus Erichson
(Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 95, 267–275.
Zu
´n
˜iga, G., Salinas-Moreno, Y., Hayes, J.L., Gre
´goire, J.C., Cisneros, R.,
2002b. Chromosome number in Dendroctonus micans and karyo-
logical divergence within the genus Dendroctonus (Coleoptera:
Scolytidae). Can. Entomol. 134, 503–510.
156 Bark Beetles
