Content uploaded by Laura Beani
Author content
All content in this area was uploaded by Laura Beani on Jul 31, 2014
Content may be subject to copyright.
Ethology Ecology & Evolution 16: 363-375, 2004
Prevalence of the parasite Strepsiptera
in adult Polistes wasps:
eld collections and literature overview
D.P. HUGHES 1,3, J. KATHIRITHAMBY 1 and L. BEANI 2
1 Department of Zoology, University of Oxford, South Parks Road, OX1 3PS, UK
2 Dipartimento di Biologia Animale e Genetica, Università di Firenze, Via Romana 17,
50125 Firenze, Italy
Received 27 October 2004, accepted 5 November 2004
The incidence of strepsipteran parasites in temperate Polistes wasps is
recorded following the collection and dissection of adults from nests, foraging sites
and hibernacula. The mean proportion of infected P. dominulus adults (i.e. para-
site prevalence) on nests was around 7%, while wasps which were captured when
hunting for prey or collecting water were rarely parasitized. Of the four Polistes
species that were recovered from overwintering aggregations (dominulus, gallicus,
nimphus and associus) only P. gallicus was uninfected. In P. dominulus, the most
numerous host sampled, up to 25% of overwintering females were infected. We
discuss our ndings in the light of an extensive collation of records of Polistes
parasitized by the strepsipteran genus Xenos in old and recent literature.
KEY WORDS: Polistes, Xenos, Strepsiptera, parasitic castrators, social insects, over-
wintering groups.
Introduction . . . . . . . . . . . . . . . . . 364
Methods . . . . . . . . . . . . . . . . . . 364
Results . . . . . . . . . . . . . . . . . . 366
Adults on the nest . . . . . . . . . . . . . . . 366
Adults at foraging sites and water sources . . . . . . . . . 366
Adults from overwintering aggregations . . . . . . . . . . 367
Discussion . . . . . . . . . . . . . . . . . 368
Parasitism of adults on the nest . . . . . . . . . . . 368
Parasitism among foraging and water collecting adults . . . . . 368
Parasitism in overwintering aggregations of Polistes . . . . . . 372
Acknowledgements . . . . . . . . . . . . . . . 373
References . . . . . . . . . . . . . . . . . 373
3 Author for correspondence: David P. Hughes, Department of Biology, University of Oulu,
Oulu 90014, Finland (Tel. +358 8 5531791; E-mail: david.hughes@oulu.).
364 D.P. Hughes, J. Kathirithamby and L. Beani
365
Stylopization of adult Polistes
INTRODUCTION
Social insects are a valuable resource for exploitation by parasites, due to the
aggregation of a large number of genetically related individuals in a central loca-
tion (SCHMID-HEMPEL 1998, NAUG & CAMAZINE 2002). Many examples of their effect
have been collected to date such as: colony-level response (HART et al. 2002, MEHDI-
ABADI & GILBERT 2002), foraging (SCHMID-HEMPEL & SCHMID-HEMPEL 1990, MORRISON
2000), colony growth (CURRIE 2001, BROWN et al. 2003) and behavioural changes
(CARNEY 1969, MÜLLER & SCHMID-HEMPEL 1993, MÜLLER 1994). Due to the high
diversity of parasites within colonies (KISTNER 1982, SCHMID-HEMPEL 1998), our
knowledge of life histories of these parasites is limited for many taxa.
A prime example of this is the order Strepsiptera, which are obligate parasitic
insects. Among the social insects, the family Stylopidae has been recorded as parasites
of wasps (Vespidae of the genera Provespa, Vespa, Vespula, Polistes, Mischocyttarus,
Belanogaster, Brachygastra, Ropalidia, Apoica, Agelaia, Chartergus, Polybia); the family
Myrmecolacidae, if males, infect the ants (Formicidae belonging to genera Campono-
tus, Crematogaster, Pheidole, Pseudomyrmex, Eciton, Solenopsis, Dolichoderus), whereas
females infect Orthoptera (see recent data in KATHIRITHAMBY & JOHNSTON 2004). In
most cases information on parasite abundance and behaviour is minimal.
Most information concerns wasps of the genus Polistes, which are popular
study tools in their own right because of their tractability and accessibility (un-
enveloped nest and wide occurrence in temperate zones, see REEVE 1991, TURILLAZZI
& WEST-EBERHARD 1996). Indeed, the rst record of an insect infected by Strep-
siptera was from P. dominulus (Christ), parasitized, i.e. ‘stylopized’ by Xenos
vesparum (ROSSI 1793). In this species, as well as in other hymenopteran hosts,
infection results in physiological castration (BRANDENBURG 1956, STRAMBI & STRAMBI
1973, MAETA & KURIHARA 1999). A recent eld and laboratory study on P. dominulus
has shown a marked change in social behaviour of stylopized wasps, leading to nest
desertion early in imaginal life and the formation of mid-season, extra-nidal aggre-
gations (HUGHES et al. 2004, BEANI et al. in press).
In a previous study on Strepsiptera, we evaluated infection levels among dif-
ferent Polistes species from Old and New World sites through dissections of imma-
tures and adults from nests (HUGHES et al. 2003). The aim of the current work is to
document the occurrence of Strepsiptera in P. dominulus, following collections and
dissections of adult wasps. Particularly, we detail parasite prevalence (proportion
of infected individuals), and parasite load (number of parasites/infected host) for
various categories of adults: (1) on the nest; (2) foraging for prey on plants and
collecting water; (3) in overwintering inter-specic groups, formed by P. dominulus,
P. gallicus, P. nimphus and P. associus. Available information on Strepsiptera infect-
ing Polistes in old and recent literature is briey reviewed, focussing particularly on
levels of parasitism across different host categories.
METHODS
Brief life-cycle of the strepsipteran genus Xenos parasitic in Polistes wasps
Infection occurs when the free-living, 1st instar larva enters a larval (or rarely egg) stage
wasp. The parasite remains endoparasitic until the host ecloses from the cell as an adult. At
364 D.P. Hughes, J. Kathirithamby and L. Beani
365
Stylopization of adult Polistes
which point both sexes of the parasite extrude the anterior region of the nal instar through
the intersegmental membranes of the host’s abdominal cuticle. Thereafter, hosts become vis-
ibly stylopized. Xenos males form puparia, from which they later emerge as free-living adults
for their short adult stage (< 5 hr). Xenos females, which are permanently neotenic endopara-
sites, extrude their cephalothorax through the intersegmental membranes of the host. Mating
and emergence of 1st instar larvae occur through the brood canal opening in the cephalotho-
rax (reviewed in KATHIRITHAMBY 1989).
The Polistes host is a primitively eusocial wasp, which in Italy begins nest foundation in
March with the rst workers emerging in May. Sexuals emerge in August-September, before
colony decline. Only female wasps (and female Xenos inside their abdomen) overwinter in
aggregations between November and March. After diapause, the female Xenos produce 1st
instar larvae which infect all the larval stages of the host (in Tuscany from May to July-
August). Emergence of stylopized workers and sexuals occurs from late May to August (see
further details in HUGHES et al. 2003).
Host collections
All collections occurred within 20 km of Florence, Italy. Collection sites (the local
names are given in Table 1) were old farmhouses, a greenhouse surrounded by elds and a
cemetery. Three categories of adult host were collected: (1) on nests; (2) prey foraging or col-
lecting water; (3) overwintering within hibernacula.
(1) Adults on the nest. Nests of P. dominulus (n = 21) were collected early in the morn-
ing under roof tiles of an abandoned property (henceforth Area 1) on 10th July (n = 7), 17th
July (n = 7) and 3rd August 2000 (n = 7). The nest was frozen within 3 hr of collection and all
adult dissected to check for signs of parasitism. Area 1 corresponds to Area C (HUGHES et al.
2003), and Area 1 (HUGHES et al. 2004).
(2) Adults at foraging sites and water sources. Wasps were captured as they ew around
plants and a water point. All collections occurred at one site (henceforth Area 2), every 2 days
between 13th July and 2nd August 2000. Flying wasps were collected as they visited a patch
of non-owering plants, i.e. without nectar and sugar sources at the time (approximately 10
m2 area abutting an abandoned house where nests were numerous). Using a sweep net, wasps
were captured if they ew very close (< 5 cm) around the stem and leaves of plants, presum-
ably seeking for prey, such as caterpillars. Typically, individuals moved around a single plant
for 5-10 sec before moving to another plant in the immediate vicinity. At the water point (1
m2 container), at the margin of the ‘foraging’ area, a net was passed close to the surface to
collect wasps as they visited the water. Wasps would alight on the water, or at the water’s edge
to drink. Collections on plants (n = 10) and at water (n = 11) lasted for 30 min, or until 10
wasps were caught. All wasps were sacriced within 3 hr and later dissected.
(3) Adults from hibernacula. Wasps were collected between the 6-10th December 2000
from 5 sites (see Table 1): old farmhouses surrounded by elds (Area 1-4); greenhouse within
ploughed eld (Area 5). Between 15-18th December 2001, collections occurred in a cemetery
(Area 6, corresponding to Area E in HUGHES et al. 2003). Overwintering sites (i.e. hibernacula)
were commonly interstices of buildings, old nests under roof tiles, but also votive candle-
holders in the cemetery site. These wasps were not dissected for signs of parasitism as X.
vesparum does not overwinter as a larval stage.
Statistical analyses
Data on parasite load (one parasite or ≥ two) and host species identity (4 species) was
analysed using binary and multinomial logistic regression analyses with the enter method,
respectively. Count data on the number of wasps on the nest or within hibernacula was ana-
lysed using ANOVA following log transformation to approximately normalize the data. All
analyses were performed using SPSS 10 and all means are shown ± SE.
366 D.P. Hughes, J. Kathirithamby and L. Beani
367
Stylopization of adult Polistes
RESULTS
Adults on the nest
In total, P. dominulus nests contained 896 adults (840 females, 56 males,
21 nests). The mean number of adults per nest was 42.67 ± 5.30 and this did not
signicantly differ among the 3 sampling weeks (ANOVA F2,20 = 0.80, P = 0.92).
The proportion of female wasps did vary with week (ANOVA F2,20 = 7.51, P = 0.04;
proportion of females = 0.99 ± 0.01, 0.97 ± 0.01 and 0.87 ± 0.05 for week 1, 2 and
3 respectively). With the exception of one nest collected on 3rd August, all nests
contained infected adults (20/21 or 0.95). The mean prevalence of infection among
adult wasps was 0.07 ± 0.02, regardless of the week of collection (Fig. 1, ANOVA
F2,20 = 2.27, P = 0.15).
Of the 61 infected adults, 7 were parasitized by 2 or more X. vesparum (69
parasites of both sexes in total, max/host = 3). The probability of parasitism by
more than one parasite was not inuenced by week of collection (Binary Logistic
Regression, Wald = 0.0015, 1 df, P = 0.97). The parasite load among infected wasps
was 1.13 ± 0.05. Only 8 of 69 parasites extruded through the host cuticle, i.e. < 1%
of the total number of adults on nests (n = 896) were visibly stylopized.
Adults at foraging sites and water sources
All wasps collected over non-owering patches and water were female P.
dominulus. Of the 63 adults captured while ying over vegetation, in manner sug-
gestive of prey searching, only one was infected (with three larval X. vesparum
males inside). Low levels of parasitism were also found among adults collected over
water: only 4 of the 88 wasps were infected. All these wasps were singly infected by
female X. vesparum releasing 1st instars at the time of capture. The degree of wing
Table 1.
The total number of wasps from overwintering aggregations according to the area of collection.
Area P. dominulus P. gallicus P. nimphus P. associus Total
wasps
Hibernacula
composition (%)
1 (Peretola) 124 (22/0.17) 87 (0) 0 0 211 59/41/0/0
2 (Montoriolo) 143 (33/0.23) 6 (0) 0 0 149 96/4/0/0
3 (Impruneta) 97 (24/0.25) 16 (0) 0 23 (2/0.09) 136 71/12/0/17
4 (Ferrone) 105 (11/0.10) 135 (0) 0 34 (0) 274 39/49/0/12
5 (Mosciano) 47 (20/0.04) 4 (0) 12 (1/0.08) 117 (0) 180 26/2/7/65
6 (Trespiano) 377 (45/0.12) 73 (0) 0 30 (3/0.10) 480 79/15/0/6
Total 893 (137/0.15) 321 (0) 12 (1) 204 (5/0.02) 1430 63/22/1/14
The gures in parenthesis are the number and proportion of parasitized wasps. Hibernacula compo-
sition lists the relative percentages of wasps according to species in this order: dominulus/gallicus/
nimphus/associus.
366 D.P. Hughes, J. Kathirithamby and L. Beani
367
Stylopization of adult Polistes
wear and tergite discoloration was extensive and suggested that these hosts were
overwintered gynes from the previous season.
Adults from overwintering aggregations
Within hibernacula, 1430 wasps were recovered and all were female (Table
1). Between 6-10th December 2000, 33 separate overwintering aggregations (from
Areas 1-5) contained 950 female Polistes of the following 4 species: P. dominulus,
gallicus (L.), nimphus (Christ) and associus Kohl. Between 15-18th December 2001,
480 female wasps (of P. dominulus, gallicus or associus) were collected from 23
overwintering aggregations (Area 6). The mean size of aggregations in hibernacula
was 25.57 wasps ± 4.81 (n = 56). The largest aggregation was 250 wasps under a
roof tile.
Table 1 shows the number and proportion of parasitized wasps for each spe-
cies of wasp collected from 6 areas. Species were not randomly distributed among
our collection sites (Multinomial Logistic regression χ2 = 366.33, 15 df, P < 0.0001).
Polistes gallicus wasps (n = 321) were all uninfected, with only one P. nimphus wasp
was parasitized (note we rarely found this species, n = 12).
In total, 143 parasitized wasps were collected from hibernacula. Parasite
number and sex is presented here for 88 P. dominulus wasps: 70 wasps were sin-
gly parasitized by a female X. vesparum; 9 had 2, and 1 had 3 female X. vesparum.
Unexpectedly, some wasps (n = 8) had male pupal stage X. vesparum or contained
empty puparia co-occurring with female X. vesparum. Males within the puparia
were dead, presumably they failed to emerge prior to host diapause. The mean par-
�
�
�
�
�
�
�
�
�
�
�
Fig. 1. — The mean prevalence (± SE) of infection of P. dominulus among adults on nests according
to collection date. The values in parenthesis are number of nests and adults dissected respectively.
368 D.P. Hughes, J. Kathirithamby and L. Beani
369
Stylopization of adult Polistes
asite load in overwintering aggregations was 1.16, comparable to the parasite load
in P. dominulus adults on nests.
DISCUSSION
Parasitism of adults on the nest
There is increasing evidence that Strepsiptera occur at high prevalence within
populations and colonies of Polistes wasps. This study was focused on P. dominu-
lus adults, and we found that all categories of hosts that were sampled were parasi-
tized, but at different levels of infection and stages of the parasite.
We found a very high proportion of infected colonies in July (20/21 or 95%)
and a relatively low parasite prevalence among adult wasps on nests (61/896, i.e.
7.1% regardless of collection date, Fig. 1). These data are in line with our previous
ndings in nests of P. dominulus collected in June and screened for endoparasitic
stages by dissection (7/12 nests and 0/45 adults, HUGHES et al. 2003, see Table 2).
Parasitized wasps leave the nest roughly one week after their emergence (HUGHES
et al. 2004). The developmental stages of the parasite corroborates early nest deser-
tion by infected wasps: 61 out of 69 X. vesparum in this sample were endoparasitic
larvae (all at 3rd-4th stage, except one at 2nd stage). Thus, the temporal window to
detect, by dissection, the infected larvae and pupae would be approximately 20 days
compared to 7-10 days to discover infected adults before they desert the nest. The
low proportion of infected colonies in P. metricus (approximately 18%, not based on
dissection: HODGES et al. 2003, see Table 2) is attributable to this clear-cut methodo-
logical difference.
Nests containing parasitized adults have been previously recorded for
Polistes from both Old and New World habitats (Table 2). Several samplings of
stylopized wasps occurred during the terminal phase of the colony (BRUES 1905,
PIERCE 1909, DUNKLE 1979, TURILLAZZI 1980), when nests may serve as a pre-
diapause aggregation site from several colonies. Thus, in those cases high rates
of infected wasps may be comparable to parasite prevalence in overwintering
groups: stylopized individuals may come from a number of nests to aggregate on
an abandoned colony.
On average, the parasite load among adults recovered from nests was approxi-
mately one Xenos per adult; which was less variable than the number of parasites
earlier detected per brood member (> 40 HUGHES et al. 2003, see also BRUES 1903
in Table 2). Whilst another study (HUGHES & KATHIRITHAMBY submitted) showed
no effect of single parasitism on the mortality of host larvae, it may be that super-
parasitized larvae either die, or are removed from the nest. This hypothesis is con-
sistent with 81% of wasps in extra-nidal aggregations being singly infected (HUGHES
et al. 2004); as well as the data presented here on parasite load among overwinter-
ing hosts (see below).
Parasitism among foraging and water collecting adults
A few studies, unfortunately, have assessed foraging ecology of Polistes (see
NANNONI et al. 2001). Our collections have shown that stylopized Polistes are rarely
368 D.P. Hughes, J. Kathirithamby and L. Beani
369
Stylopization of adult Polistes
Table 2.
A survey of parasitized Polistes wasps from the literature, according to host category.
References Host / Location Notes on infected wasps Method Prevalence
Collections of adults away from the nest
ROSSI 1793 P. dominulus / France rst account of a strepsipteran [EP] —
HORN 1871 P. hebraeus F. / India
P. stigma (F.) / India
superparasitism
‘many’ infected [EP] 0.20
—
AUSTIN 1882 P. metricus Say / MA 2/14 ¢in and 7/36 ™in (Aug) [EP] 0.14, 0.19
HUBBARD 1892 P. fuscatus (F.) / VA 1 ™in “hiding” under bark [EP] —
BRUES 1903 P. texanus* / TX 1 ™in with empty pupa [EP] —
BRUES 1905 P. annularis (L.) / TX
P. rubiginosus* / TX
7 ™in with empty pupae
1 ™in with female releasing 1st instars (May)
—
—
PIERCE 1909: 21
P. pallipes (Lep ) / MA
P. metricus / OH
P. rubiginosus* / DC
P. rubiginosus* / TX
6 ™in, 4 ¢in with 30 Xenos (Sep)
10 ™in; 4 ¢in with 38 Xenos (Jun-Sep, over 5 years)
1 ™in with 8 females and 1 ™in with empty puparia
1 ™in with 6 empty pupae (Jul)
[EP]
—
—
—
—
WHEELER 1910 P. metricus / CT 1000 wasps on owers (14-29th Aug 1900) [EP/D] 0.29
PIERCE 1918: 393
P. aurifer Saussure / CA
P. anaheimensis* / CA
P. annularis / NE
P. bellicosus Cresson / AZ
P. variatus Cresson / MD
1 ™in with larvipositing female (Aug)
1 ™in with female
7 ™in with 52 males and 6 females Xenos (Aug)
1 ™in with 4 pupae (Aug)
5 ™in 4 with one female, 1 with pupa (Nov)
[EP]
—
—
—
—
—
BRÈTHES 1923 P. cavaptya Saussure / Argentina
P. versicolor (Olivier) / Argentina — [EP] —
—
RICHARDS & RICHARDS 1951 P. testaceicolor Bequaert / Guiana
P. carnifex (F.) / Guiana
‘heavily stylopized’ [EP] —
—
(continued)
370 D.P. Hughes, J. Kathirithamby and L. Beani
371
Stylopization of adult Polistes
References Host/Location Notes on infected wasps Method Prevalence
OLIVEIRA & KOGAN 1962
P. canadensis (L.)
P. melanosoma Saussure
P. versicolor
P. spp. (?) / (all Southern Brazil)
10 ™in in total for 4 host species [EP]
—-
—
—
RIEK 1970 P. variabilis (F.) / Australia
P. tepidus (F.) / Australia — [EP] —
—
KIFUNE 1979 P. lanio lanio (F.) / Peru 4 ™in ying around building (Aug-Sep) [EP/D] —
FOWLER & PARRISH 1982 P. fuscatus / NJ 8 ¢in aggregated on a eave (Jul) [EP] 1.00
KIFUNE 1983 P. crinitus (Felton) / Virgin Islands 1 ™in and 1 ¢in around buildings (Nov-Jun) [EP] —
KIFUNE & MAETA 1985 P. rothneyi gressitti Van der Vecht
P. gigas (Kirby) / Taiwan
3 ™in
1 ™in [EP/D] —
—
POLAK 1993 P. canadensis / Costa Rica several ¢in at leks (May-Sep) [EP] 0.05
PICKETT & WENZEL 2000 P. fuscatus / NY several ™in on owers (K. PICKETT pers. comm.) [EP/LO] 0.16 (n=68),
0.18 (n=44)
HUGHES et al. 2003 P. carnifex / Mexico 1 ™in with larvipositing female; 1 ™in with pupal males
on vegetation (Apr) [EP] —
Collections of adults on the nest
HUBBARD 1892 P. americanus* / FL
1 nest: ™in were lethargic and did not forage. Some
had 8 or 10 parasites. In lab >100 male Xenos bred out
(Jun-Jul)
[EP/LO] —
BRUES 1903 P. annularis / TX 1 of 4 nests infected. 4 ™i n reared out in lab [EP/LO/D] —
SKINNER 1903 P. texacanus* / TX 2 nests: 34/144 wasps parasitized (Sep) [EP] 0.23
BRUES 1905 P. annularis / TX
1 nest: 44/86 ™in; 91 Xenos (Jul)
1 nest: 36/42 ™in; 118 Xenos and some empty puparia
(Oct)
[EP/D]
[EP/LO/D]
0.51
0.85
Table 2. (continued)
(continued)
370 D.P. Hughes, J. Kathirithamby and L. Beani
371
Stylopization of adult Polistes
References Host/Location Notes on infected wasps Method Prevalence
PIERCE 1909: 17
PIERCE 1909: 16
PIERCE 1909: 21
P. annularis / TX
P. minor Palisot de Beauvois / TX
P. minor / TX
2 large nests (84% males, Sep)
2/4 nests: 1/26 and 5/191 wasps (Sep)
1/2 nests: 1/17 wasps (Oct)
[EP]
0.20
0.04, 0.03
0.06
FITZGERALD 1938 P. pacicus (F.) / Trinidad 1 nest: all stylopized (12) and lethargic (no date) [EP] 1.00
DUNKLE 1979 P. annularis / FL many nests, only males examined: 569/11542 ¢in (Oct/
Nov) [EP] 0.05
TURILLAZZI 1980 P. gallicus / Italy ™in by Xenos females Sep/Nov) [EP] 0.19
STRASSMANN 1981 P. exclamans Viereck / TX 8 of “tens of thousands” examined were stylopized [EP] —
HODGES et al. 2003 P. metricus / GA 51 of 303 early season nests infected by X. peckii [LO] 17.85
Collections of overwintering females
PIERCE 1909: 20 P. annularis / FL 6/60 (Nov); 4/54 (Nov); 2/35 (Jan). ™in, plus 2 ™in with
empty pupae [EP] 0.10, 0.07, 0.05
TURILLAZZI 1980 P. dominulus / Italy 4 groups on nests under tiles [EP] 0.23
Collections of immature wasps
BRUES 1903 P. annularis / TX 1 larva contained 31 parasites [D]
BRUES 1905 P. annularis / TX 2 nests: 1/12 (Sept) [D] 0.08
HUGHES et al. 2003
P. dominulus / Italy
P. gallicus / Italy
P. carnifex / Mexico
P. stabilinus / Mexico
7 of 12 nests: 44/261 immatures
4 of 10 nests: 45/154 immatures
4 of 8 nests: 9/77 immatures
2 of 15 nests: 5/400 immatures
[D]
0.17
0.29
0.12
0.01
Table 2. (continued)
Species names as supplied in original publication: * indicates possible invalid names. The list is not exhaustive (see HUGHES 2003). Where possible,
relevant notes are presented such as: host/parasite sex, proportion of infected wasps and nests, and date of collection. The abbreviations in ‘method’
refer to parasite detection: EP = Evidently Parasitized (without dissection); LO = Lab Observation, adults reared in cage; D = Dissection of at least
some individuals to check for endoparasitic stages. The symbols ™in = infected female and ¢in = infected male. The USA state names in Location col-
umn are abbreviated.
372 D.P. Hughes, J. Kathirithamby and L. Beani
373
Stylopization of adult Polistes
encountered around non-owering vegetation, which were assumed to be foraging
sites for proteinaceous food (e.g. caterpillars) to developing larvae: only one infect-
ed individual was recovered from 63 wasps sampled. This observation corroborates
previous ndings that infected wasps neither forage nor feed brood (HUGHES et al.
2004); but interestingly they do eat larval ies (maggots) brought to the nest by for-
agers, as well as sugar and honey (pers. obs.). In bumblebees, where infected work-
ers may forage for their colony, the presence of parasites more subtly affects ower
choice and pollen loads (SCHMID-HEMPEL & SCHMID-HEMPEL 1990, SCHMID-HEMPEL &
MULLER 1991, SCHMID-HEMPEL & STAUFFER 1998).
Our study did not record the occurrence of stylopized wasps around sugar
sources such as owers, fruit or tree-sap, though they were often seen there
(pers. obs.). A highly scattered distribution of owering patches discouraged this
approach in our study areas. Many records of stylopized wasps away from the nest
do exist but in most cases no details have been furnished (Table 2). Special note
should be made of the mammoth collection of 1,000 P. metricus over 10 days from
owers by WHEELER (1910) who recoded a 45% infection level in the rst 4 days.
This level was probably higher, as only a small number were dissected to check for
endoparasitic stages. Stylopized individuals of a further North American species (P.
fuscatus) were also collected from owers at relatively high levels (16-18%) (PICKETT
& WENZEL 2000, and pers. comm.). Both these records may reect a similar occur-
rence of early nest desertion by stylopized individuals in these species as well as in
P. dominulus.
Interestingly, all the stylopized wasps around a water container (4/88, i.e.
4.5%) were infected by a larvipositing female X. vesparum. Some morphological
cues indicated that these wasps were old, overwintered females. The release of 1st
instars at water could be a way to reduce desiccation of the primary stages whilst
allowing encounters with phoretic agents (water-collecting workers).
Parasitism in overwintering aggregations of Polistes
Our data conrm previous observations that diapausing aggregations of
Polistes may be multispecic and are composed principally of female wasps (BRIM-
LEY 1908, REED & LANDOLT 1991, HUNT et al. 1999). A strong area effect of the likeli-
hood of belonging to a particular Polistes species (Table 1) suggests a patchy com-
position of species within Tuscan populations.
For P. dominulus, parasite prevalence was surprisingly high, ranging from 4 to
25% (Table 1). These data were in agreement with the few previous records which
exist (see Table 2: 0.05-0.23 PIERCE 1909, TURILLAZZI 1980). This scarcity could reect
the cryptic nature of parasitism at this stage. That is, the visible portion (cephalo-
thorax) of female strepsipterans is dorsoventrally attened and hidden between the
tergites. Thus, stylopization is less conspicuous than in case of large male puparia,
which we rarely found in overwintering wasps (this study and PIERCE 1909).
Prevalence was very low in our limited sample of P. nimphus (1/12) as well
as in the more regularly encountered species, P. associus (5/204). This is the rst
record, to our knowledge, of stylopized P. associus wasps. Unexpectedly, P. gallicus
was not found to be parasitized although this species was collected in high num-
bers (n = 321) in these winter collections. This contrasts with a high proportion of
nests and brood being infected (HUGHES et al. 2003). P. gallicus adults might repre-
sent a secondary and not suitable host for X. vesparum.
372 D.P. Hughes, J. Kathirithamby and L. Beani
373
Stylopization of adult Polistes
Because strepsipterans are parasitic castrators, the very high prevalence
among hibernacula occupants means that up to 25% of overwintering P. dominulus
wasps do not take part in nest foundation. In a recent report on the prevalence of
strepsipteran parasitism among overwintering Vespa analis, the authors showed that
between 8-15% of queens were infected but claimed that this level is not expected
to have a serious effect on population dynamics of their hosts (TATSUTA & MAKINO
2003).
This study, and recent work, have revealed hitherto unappreciated levels of
parasitism among Polistes by Strepsiptera. A review of the literature highlighted 31
known hosts among Polistes (32, including our rst record for P. associus). Despite
their wide distribution and high levels in some species, it remains difcult to make
inferences on the effect of parasitism at the colony and population levels. Future
work should attempt empirical investigations. Strepsiptera are useful tools with
which to do this as they are: relatively easy and inexpensive to sample; tractable
to laboratory manipulations; and found in wide range of social and non-social
Hymenoptera, which permits inter-taxa comparison of their effects.
ACKNOWLEDGMENTS
We thank Emily Caruso and Anna Seward for help in the eld and Stefano Turillazzi,
Francesco Dessì-Fulgheri and members of the Florence Group for the Study of Social Wasps
for their hospitality. D. Hughes was supported by the Hope Studentship in Entomology
(Oxford University and Jesus College, Oxford). The work was funded by the Royal Society
Travel Joint Project grant (22335) to Jeyareney Kathirithamby.
REFERENCES
AUSTIN J.D. 1882. Collecting Sylopidae. Journal of the Boston Zoological Society 1: 12-13.
BEANI L., HUGHES D.P., TURILLAZZI S. & KATHIRITHAMBY J. (in press). Parasitic castation does
not promote social behaviour in paper wasps. Social Insect Life 5.
BRANDENBURG J. 1956. Das endokrine System des Kopfes von Andrena vaga Pz. (Ins.
Hymenopt.) und Wirkung der Stylopisation (Stylops, Ins. Strepsipt.). Zeitschrift für Mor-
phologie und Ökologie der Tiere 45: 343-364.
BRÈTHES J. 1923. Primera contribución para el conocimiento de los “Strepsiptera” argentinos.
Revista de la Facultade de Agronomia Universidad Nacional de La Plata 15: 41-56.
BRIMLEY C.S. 1908. Male Polistes annularis survive the winter. Entomological News 8: 107.
BROWN M.J.F., SCHMID-HEMPEL R. & SCHMID-HEMPEL P. 2003. Strong context-dependent viru-
lence in a host-parasite system: reconciling genetic evidence with theory. Journal of Ani-
mal Ecology 72: 994-1002.
BRUES C.T. 1903. A contribution to our knowledge of the Stylopidae. Zoologische Jahrbücher
(Anatomie) 18 (2): 241-270.
BRUES C.T. 1905. Notes on the life history of the Stylopidae. Biological Bulletin 8: 290-295.
CARNEY W.P. 1969. Behavioral and morphological changes in carpenter ants harbouring dicro-
coeliid metacercariae. The American Midland Naturalist 82: 605-611.
CURRIE C.R. 2001. Prevalence and impact of a virulent parasite on a tripartite mutualism.
Oecologia 128: 99-106.
DUNKLE S.W. 1979. Sexual competition for space of the parasite Xenos pallidus Brues in male
Polistes annularius (L.) (Strepsiptera, Stylopidae, and Hymenoptera, Vespidae). Psyche
86: 327-336.
374 D.P. Hughes, J. Kathirithamby and L. Beani
375
Stylopization of adult Polistes
FITZGERALD D.V. 1938. Social wasps (Hym., Vespidae) from Trinidad with a note on the genus
Trypoxulon Latreille. Transactions of the Royal Entomological Society of London 87: 181-
191.
FOWLER H.G. & PARRISH M.D. 1982. Extra-nidal aggregation of stylopized paper wasp males.
Journal of the Georgia Entomological Society 17: 446-447.
HART A.G., BOT A.N.M. & BROWN M.J.F. 2002. A colony-level response to disease control in a
leaf-cutting ant. Naturwissenschaften 89: 275-277.
HODGES A.C., HODGES G.S. & ESPELIE K.E. 2003. Parasitoids and parasites of Polistes metricus
Say (Hymenoptera: Vespidae) in Northeast Georgia. Annals of the Entomological Society
of America 96: 61-64.
HORN C. 1871. Notes on the habits of some hymenopterous insects from the northwest prov-
inces of India. Transactions of the Zoological Society of London 7: 170-172.
HUBBARD H.G. 1892. The life history of Xenos. Canadian Entomologist 24: 257-261.
HUGHES D.P., BEANI L., TURILLAZZI S. & KATHIRITHAMBY J. 2003. Prevalence of the parasite
Strepsiptera in Polistes as detected by dissection of immatures. Insectes Sociaux 50 (1):
62-69.
HUGHES D.P. & KATHIRITHAMBY J. (submitted) Cost of strepsipteran macroparasitism for imma-
ture wasps: Does sociality modulate virulence? Behavioural Ecology.
HUGHES D.P., KATHIRITHAMBY J., TURILLAZZI S. & BEANI L. 2004. Social wasps desert the colony
and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15:
1037-1043.
HUNT J.H., BRODIE R.J., CARITHERS T.P., GOLDSTEIN P.Z. & JANZEN D.H. 1999. Dry season migra-
tion by Costa Rican lowland paper wasps to high elevation cold dormancy sites. Bio-
tropica 31: 192-196.
KATHIRITHAMBY J. 1989. Review of the Order Strepsiptera. Systematic Entomology 14: 41-92.
KATHIRITHAMBY J. & JOHNSTON J.S. 2004. The discovery after 94 years of the elusive female of
a myrmecolacid (Strepsiptera), and the cryptic species Caenocolax fenyesi Pierce sensu
lato. Proceedings of the Royal Society (B) (Suppl.) 271: S5-S8.
KIFUNE T. 1979. A new species of the genus Xenos from Peru (Strepsiptera: Stylopidae). Kon-
tyû 47 (3):403-411.
KIFUNE T. 1983. Two new species of the family Stylopidae (Strepsiptera) parasitic on Polistes and
Pachodynerus (Hymenoptera) from the Virgin Islands, West Indies. Kontyû 51: 330-338.
KIFUNE T. & MAETA Y. 1985. Taxonomical studies on the genus Xenos (Strepsiptera, Stylopidae)
parasitic on Vespa and Polistes (Hymenoptera, Vespidae) of Taiwan with descriptions of
three new species (Notulae Strepsipterologicae-XIV). Kontyû 53 (3): 426-435.
KISTNER D.H. 1982. The social insects’ bestiary, pp. 1-244. In: Hermann H.R., Edit. Social
insects. New York: Academic Press.
MAETA Y. & KURIHARA M. 1999. Effects of stylopization on the ovarian development of host
wasp, Bembicinus bimaculatus, parasitized by Paraxenos nagatomii (Strepsiptera, Sty-
lopidae). Kontyû 13: 1-8.
MEHDIABADI N.J. & GILBERT L.E. 2002. Colony-level impacts of parasitoid ies on re ants.
Proceedings of the Royal Society of London Series (B) 269: 1695-1699.
MORRISON L.W. 2000. Mechanisms of Pseudacteon parasitoid (Diptera: Phoridae) effects on
exploitative and interference competition in host Solenopsis ants (Hymenoptera: Formi-
cidae). Annals of the Entomological Society of America 93: 841-849.
MÜLLER C.B. 1994. Parasitoid induced digging behavior in bumblebee workers. Animal Behav-
iour 48: 961-966.
MÜLLER C.B. & SCHMID-HEMPEL P. 1993. Exploitation of cold temperature as defense against
parasitoids in bumblebees. Nature 363: 65-67.
NANNONI A., CERVO R. & TURILLAZZI S. 2001. Foraging activity in European Polistes wasps
(Hymenoptera: Vespidae). Bollettino della Società Entomologica Italiana 133 (1): 67-78.
NAUG D. & CAMAZINE S. 2002. The role of colony organization on pathogen transmission in
social insects. Journal of Theoretical Biology 215: 427-439.
OLIVEIRA S.J.D. & KOGAN M. 1962. New records about Brazilian Strepsiptera (Insecta). Memo-
rias do Instituto Oswaldo Cruz 58: 183-187.
374 D.P. Hughes, J. Kathirithamby and L. Beani
375
Stylopization of adult Polistes
PICKETT K.M. & WENZEL J.W. 2000. High productivity in haplometrotic colonies of the intro-
duced Paper wasp Polistes dominulus (Hymenoptera: Vespidae; Polistinae). Journal of
the New York Entomological Society 108: 314-325.
PIERCE D.W. 1909. A monographic revision of the twisted winged insects comprising the order
Strepsiptera Kirby. Bulletin of the U.S. National Museum 66: 1-232.
PIERCE D.W. 1918. The comparative morphology of the order Strepsiptera together with
records and descriptions of insects. Proceedings of the United States National Museum
54 (2242): 391-501.
POLAK M. 1993. Competition for landmark territories among male Polistes canadensis (L.)
(Hymenoptera, Vespidae): large-size advantage and alternative mate acquisition tactics.
Behavioral Ecology 4: 325-331.
REED H.C. & LANDOLT P.J. 1991. Swarming of paper wasp (Hymenoptera, Vespidae) sexuals at
towers in Florida. Annals of the Entomological Society of America 84: 628-635.
REEVE H.K. 1991. Polistes, pp. 99-148. In: Ross K.G. & Matthews R.W., Edits. The social biol-
ogy of the wasps. Ithaca: Cornell University Press.
RICHARDS O.W. & RICHARDS M.J. 1951. Observations on the social wasps of South America
(Hymenoptera Vespidae). Transactions of the Royal Entomological Society of London
102: 1-117.
RIEK E.F. 1970. Strepsiptera, pp. 622-635. In: Mackerras I.M., Edit. Insects of Australia. A
textbook for students and research workers. Canberra: Melbourne University Press
ROSSI P. 1793. Observation de M. Rossi sur un nouveau genre d’lnsecte, voisin des Ichneu-
mons. Bulletin de la Société Philomathique de Paris 1: 49.
SCHMID-HEMPEL P. 1998. Parasites in social insects. Princeton: Princeton University Press.
SCHMID-HEMPEL P. & SCHMID-HEMPEL R. 1990. Endoparasitic larvae of conopid ies alter pol-
lination behavior of bumblebees. Naturwissenschaften 77: 450-452.
SCHMID-HEMPEL P. & STAUFFER H.P. 1998. Parasites and ower choice of bumblebees. Animal
Behaviour 55: 819-825.
SCHMID-HEMPEL R. & MÜLLER C.B. 1991. Do parasitized bumblebees forage for their colony.
Animal Behaviour 41: 910-912.
SKINNER H. 1903. (Editorial note on Xenos). Entomological News 14: 274.
STRAMBI A. & STRAMBI C. 1973. Inuence du développement du paraiste Xenos vesparum
Rossi (Insecte, Strepsitere) sur le système neuroendocrinien des femelles de Polistes
(Hyménoptère, Vepside) au debut de leur vie imaginale. Archives d’Anatomie Micro-
scopique et de Morphologie Expérimentale 62 (1): 39-54.
STRASSMANN J.E. 1981. Parasitoids, predators, and group size in the paper wasp, Polistes excla-
mans. Ecology 62: 1225-1233.
TATSUTA H. & MAKINO S. 2003. Rate of strepsipteran parasitization among overwintered
females of the hornet Vespa analis (Hymenoptera: Vespidae). Environmental Entomology
32 (1): 175-179.
TURILLAZZI S. 1980. Seasonal variations in the size and anatomy of Polistes gallicus (L.)
(Hymenoptera, Vespidae). Monitore Zoologico Italiano 14: 63-75.
TURILLAZZI S. & WEST-EBERHARD M.J. 1996. Natural history and evolution of Paper-wasps.
Oxford: Oxford University Press.
WHEELER W.M. 1910. The effects of parasitic and other kinds of castration in insects. Journal
of Experimental Zoology 8: 377-438.
