Avian growth and development. Evolution in the altricial precocial spectrum

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1.1. Intr1.1. Intr
1.1. Intr1.1. Intr
1.1. Introductionoduction
oductionoduction
oduction
Since the Late Triassic, the time of
Protoavis texensis
(Chatterjee 1991), over 200 million years of evolution-
ary diversification of birds have resulted in about 8900
living species. Rather than there being a gradual and
continuous diversification of birds, recent paleonto-
logical perspectives suggest that most avian lineages
produced during the Mesozoic did not survive the
extinctions at the end of the Cretaceous period and
that most recent lineages arose in a second, almost
explosive phyletic radiation during a relatively short
period of 10 million years in the early Tertiary (Chiappe
1995; Feduccia 1995).
Among other attributes of avian diversity, this ra-
diation produced the broad spectrum of development
patterns that we see in contemporary birds. The chicks
of various species of bird differ markedly in the rela-
tive degree of maturation of many aspects of their
behavior, physiology, and anatomy. The functional
maturity of the chick at any point in its postnatal de-
velopment is closely tied to the care it receives from
its parents, and probably also to many aspects of its
environment. Variation among taxa in the developmen-
tal trajectory of this suite of attributes has led orni-
thologists to separate birds into altricial and precocial
developmental types. Designation of a species into one
or the other category has been based largely on the
condition of the hatchlings.
The attributions
nidifugous
and
nidicolous
1 were
introduced when Oken (1816) referred to
Nestflüchter
(nest-fleers, or nidifugous birds) and
Nesthocker
(nest-
squatters, or nidicolous birds). The terms
Aves altrices
and
Aves precoces
2 were introduced into ornithology
by Sundeval (1836), who had based his classification
of birds on the earlier study by Oken (1816). The origi-
nal usages of
altricial
and
nidicolous
were synony-
mous, as were those of
precocial
and
nidifugous
. To-
day, these pairs of terms are used in slightly differing
contexts, although their general meanings overlap in
some aspects.
Altricial
and
precocial
primarily refer
to the developmental stage of the chick, whereas
nidicolous
and
nidifugous
refer to nest attendance.
11
11
1PP
PP
Paa
aa
attertter
ttertter
tterns of Dens of De
ns of Dens of De
ns of Devv
vv
velopment:elopment:
elopment:elopment:
elopment:
TT
TT
The he
he he
he AltrAltr
AltrAltr
Altricial-Pricial-Pr
icial-Pricial-Pr
icial-Precocial Spectrecocial Spectr
ecocial Spectrecocial Spectr
ecocial Spectrumum
umum
um
J. Matthias Starck and Robert E. Ricklefs
Additional terms have since been introduced to de-
scribe different syndromes of developmental maturity
of hatchlings, parent-chick interactions, and chick-
environment interactions (see Table 1.1 and the fol-
lowing discussion).
This chapter considers the altricial-precocial spec-
trum on several comparative levels. We discuss the
various schemes by which developmental patterns,
particularly the developmental state of the neonate, are
classified at present. We then briefly review the his-
tory of avian systematics with special reference to the
use of mode of development as a basis for classifying
birds and the influence of classifications on thinking
about the evolution of avian development. We consider
evidence from the fossil record of neonates of birds
and their phylogenetic outgroups to determine whether
the altricial or the precocial state was ancestral in the
evolution of avian ontogenies. We present a new analy-
sis of the altricial-precocial spectrum based exclusively
on physiological characters of the neonate, without
consideration of such context-specific behaviors as
locomotory activity and parent-offspring relations. We
undertake this analysis to determine whether, in a de-
velopmental sense, the altricial-precocial “spectrum”
has a single dimension or is multivariate and to see
whether taxa are uniformly and continuously distrib-
uted along the spectrum or clustered in certain regions.
The results of these analyses will influence our inter-
pretation of the evolutionary diversification of devel-
opmental patterns. Finally, a glimpse of mammalian
developmental patterns provides some comparative
insights into the evolution of ontogenies in vertebrates
and allows us to find out specific attributes of evolu-
tionary diversification of ontogenies in both birds and
mammals.
1.2. Classif1.2. Classif
1.2. Classif1.2. Classif
1.2. Classificaica
icaica
ication of Hation of Ha
tion of Hation of Ha
tion of Hatctc
tctc
tchlingshlings
hlingshlings
hlings
The altricial-precocial spectrum extends from song-
birds and parrots, whose chicks hatch in an almost
embryolike state, on the one extreme, to the mega-
podes, whose hatchlings resemble adult birds and can
fly from the first day after hatching, on the other ex-
treme. Traditional classifications of development pat-
terns recognize several categories arranged along an
altricial-precocial gradient according to a combination
of morphological and behavioral characteristics of the
neonates. The basic differentiation and character de-
1
Nidi
-: from the Latin
nidus,
“nest”; -
fugous
: from the Latin
fugere,
“flee”;
-colous
:
from the Latin
colere,
“inhabit.”
2
Aves
(pl.): from the Latin
avis,
“bird”;
altrices
:
from the
Latin
altrix,“
wet nurse”;
precoces
: from the Latin
praecoquis
,
“early maturing.”
3
reprinted from
reprinted from: Avian Growth and Development. Evolution within the altricial precocial spectrum. J. M.
Starck and R. E. Ricklefs (eds). Oxford University Press, New York, 1998

4
Table 1.1. Commonly used synonyms for precocial and altricial hatchlings
Portmann
(1935) Nice (1962) Skutch (1976) Most others J.M.Starck
(1993) 123456789abSome examples
Gruppe 1 Precocial 1 Superprecocial Superprecocial Megapodiidae
Precocial 2 Precocial Precocial Precocial 1 Anatidae, man
y
charad
r
Gruppe 2 Precocial 3 Precocial 2 Rheidae, Numididae, P
Melea
g
rididae, Tetrao
n
Precocial 4 Subprecocial Semi-
precocial Precocial 3 Cracidae, Turnicidae,
R
Gruidae
Gruppe 3 Semiprecocial Semialtricial Semiprecocial many Alcidae, Laridae
,
Stercorariidae
Gruppe 4 Semialtricial 1 Semialtricial Semialtricial Accipitridae, Ciconiid
a
Gruppe 5 Semialtricial 2 Altricial Altricial Altricial 1 Columbidae, Phaethon
t
Phalacrocoracidae
Gruppe 6, 7 Altricial Altricial 2 Sulidae, Psittacidae, P
a
1. Downy hatchling plumage 7. Stay in nest
2. Motor activity 8. Eyes closed at hatching
3. Locomotor activity 9. Without external feathers at hatching
4. Follow parents a. No parent-chick interaction
5. Search food and feed alone b. Contour feathers at hatching
6. Young fed by parents

scription goes back to Oken (1837), who said of altricial
birds that “they come naked and blind into the world,
needing to be fed in the nest.”3 Of precocial birds, Oken
stated that “the young come from the egg with sight
and feathered; not being fed, but soon running about
and searching for their food by themselves.”4 This ba-
sic distinction between altricial and precocial has not
changed to the present (Nice 1962; Ricklefs 1983;
O’Connor 1984; J.M. Starck 1993).
“Superprecocial” megapodes (Fig. 1.1a) occupy the
precocial extreme of the spectrum. The young are to-
tally independent of their parents, and in some species
the chicks can fly from the first day of postnatal life
(Table 1.1). As already recognized by Stresemann
(1927 – 1934), megapode superprecocity continuously
grades into the precocity typical of galliform species,
whose hatchlings seek their own food and depend on
their parents only for protection and brooding. Thus,
Nice (1962) distinguishes megapodes as precocial-1
and galliforms as precocial-2 or precocial-3. Ostriches,
ducks (Fig. 1.1b), geese, jacanas, and many shorebirds
exhibit a similar independence and usually are placed
in the precocial-2 category of Nice. In some of the
Galliformes (e.g., most Meleagrididae and Tetra-
onidae), parents find food items and point them out to
their chicks on each foraging excursion. These taxa
are placed in a lower category of precocity (precocial-3
of Nice). Chicks of cranes, rails, grebes, loons,
bustards, and button quails (Fig. 1.1c) display a pre-
cocial development of mobility and sensory organs,
but their parents offer them food for some time (often
one to two weeks) after hatching (precocial-4 of Nice;
see Table 1.1 for classification by different authors).
The young of many alcids, gulls, and terns (Fig. 1.1d)
are described as semiprecocial5 because of their rela-
tively less developed locomotor activity, stronger nest
attendance, and complete dependence on the parents
for food. Within a few days after hatching semipre-
cocial chicks do undertake excursions around the nest
to hide in vegetation, but they return to the nest to be
fed by their parents.
Species whose chicks remain in the nest for much
or all of their development are refered to as altricial or
nidicolous. Among them, raptors (Fig. 1.1e), storks,
herons, and many other families are designated as
semialtricial-1 because neonates are densely covered
by down and have open eyes; semialtricial chicks are
relatively active soon after hatching. Fully altricial
hatchlings hatch with closed eyes and exhibit little
motor activity other than begging. Some altricial chicks
hatch with natal down (Fig. 1.1f; semialtricial-2 of Nice
1962), others hatch without externally visible feathers
(Fig. 1.1g). The presence (ptilopaedic6) or absence of
feathers (gymnopaedic7) has been used to further dis-
tinguish between altricial-1 and altricial-2 in J.M.
Starck’s (1993) classification, which are equivalent to
semialtricial-2 and altricial in Nice’s scheme. Whether
the intermediate category is called semialtricial-2 or
altricial-1 depends on the relative importance placed
on feathering compared to vision (Table 1.1).
Traditionally, the altricial-precocial spectrum has
been characterized by a heterogeneous set of charac-
ters including behavior (nest attendance; feeding
behavior), parent-chick relationships, and purely ana-
tomical traits (eyes open or closed; presence of natal
down). These traits do not easily align themselves in a
continuous sequence. Furthermore, because they in-
clude categorical traits that lack continuous distribu-
tions and have an uncertain relationship to the devel-
opmental state of the chick, they make comparisons
among species and interpretations of evolutionary di-
versification difficult. Expression of some of the traits,
particularly nest leaving and self-feeding, depend on
nest site and food supply and may therefore be inde-
pendent of development per se. Most classifications
of neonates, including that of Nice (1962), are one-
dimensional even though they are based on several
characters: that is, developmental classes may be or-
dered so that the state of any one character predicts
the state of all other characters preceding it in the pro-
gression. For example, all species that leave the nest
at hatching have a downy plumage and open eyes; all
species that are self-feeding leave the nest at hatching
and have a downy plumage; and so on. Table 1.1 lists
the characters frequently used in classifications of bird
hatchlings. These include considerable redundancy
(e.g.,
locomotory activity
versus
stay in nest
), change
in polarity (
eyes closed,
altricial;
follow parents
, pre-
cocial), and ambiguity about what is a character and
what is a character state (e.g.,
fed by parents
,
follow
parents
, and
search for food alone
could be states of
the single character
feeding
). Most classifications use
up to nine different characters to describe the develop-
mental mode of avian hatchlings. Here, we look more
closely at how these characters have been applied to
ascertain their consistency and utility. We use the ter-
minology of Nice for reference.
The first character,
downy hatchling plumage
, dis-
Patterns of Development: The Altricial-Precocial Spectrum 5
3 “Sie kommen nackt und blind zur Welt; bedürfen der Aetzung
im Nest” (p. 24).
4 “Die Jungen kommen sehend und mit Federn aus dem Ey,
werden nicht geätzt, sondern laufen bald herum und suchen
ihr Futter selbst” (p. 380).
5 “Platzhocker” of Peters and Müller (1951).
6
Ptilo
-: from the Greek, πτιλοσ, “feather”;
paedic
: from the
Greek παισ, “child.”
7
Gymno-
: from the Greek (γυµνοσ, “naked”;
paedic
: from
the Greek παισ, “child.”

(a) (b)
(c) (d)
(e) (f)
6

7Patterns of Development: The Altricial-Precocial Spectrum
FF
FF
Figig
igig
ig. 1.1. . 1.1.
. 1.1. . 1.1.
. 1.1. (a) Precocial-1 hatchling of a brush turkey,
Alectura
lathami
(courtesy of E. Sutter, Basel). (b) Precocial-2
hatchling of Muscovy duck,
Cairina moschata
. (c) Preco-
cial-4 hatchling of Japanese crane,
Grus japonica
in Frank-
furt Zoo. (d) Semiprecocial hatchling of Forster’s tern,
Sterna
forsteri
. (e) Semialtricial-1 hatchling of Eurasian kestrel,
Falco tinnunculus
. (f) Semialtricial-2 hatchling of rock pi-
geon,
Columba livia
f. dom. (g) Altricial hatchling of rice
finch,
Lonchura oryzivora
[All photos by J.M. Starck, ex-
cept (a)].
occurs both in altricial and in precocial groups and
thus does not distinguish between them. The seventh
character,
stay in the nest
, is the opposite of character
three,
locomotor activity
, and therefore not an inde-
pendent developmental character. It also refers to the
nest attendance rather than to the developmental stage
of the chick and in some groups, such as alcids, may
reflect constraints of the nest site rather than the chick’s
ability to walk. The eighth character,
eyes closed at
hatching
, is diagnostic for altricial hatchlings and may
be indicative of the developmental stage of the nerv-
ous system. The ninth character,
hatch without exter-
nally visible feathers
, distinguishes a small subset of
altricial hatchlings, but the character seems to be ex-
tremely variable and is probably not indicative of the
state of development (see chapter 3).
The presence or absence of feathers at hatching may
vary among related taxa or even within families. For
example, within suboscine passerine birds the bearded
bellbird (
Procnias averano,
Cotingidae) hatches with
a dense cover of natal down (Snow 1970) and the east-
ern kingbird (
Tyrannus tyrannus
, Tyrannidae) is
densely covered with natal down, whereas many oth-
ers hatch naked (Skutch 1976). Within swallows
(Hirundinidae), the barn swallow (
Hirundo rustica
) and
the cliff swallow (
Petrochelidon pyrrhonota
) have na-
tal down, but the purple martin (
Progne subis
) hatches
naked (Wetherbee 1957). Within corvids, the yellow-
billed chough (
Pyrrhocorax graculus
) hatches with a
dense cover of natal down, but the red-billed chough
(
Pyrrhocorax pyrrhocorax
) hatches almost naked.
Clark’s nutcracker (
Nucifraga columbiana
) and Ameri-
tinguishes altricial (without down) from all other de-
velopmental categories. However, marked variability
in the presence of down among close relatives (see the
following) makes this an inconsistent and ambiguous
trait. The second character,
motor activity,
is difficult
to categorize because all neonates “move” to some
extent, if only to beg for food. The third character,
locomotor activity
, referring to the ability to leave the
nest at an early age, separates the two major develop-
mental groups, altricial and precocial. We have already
suggested that nest leaving is context-dependent, how-
ever, and may not correspond exactly to the develop-
mental state of the neonate. In particular, many
seabirds, especially Procellariiformes, remain in the
nest and are classified by Nice (1962) as semialtricial,
although they are physiologically advanced in heat
production. The fourth character,
follow parents,
is also
context-dependent according to the nature of the food
resources and habitat. The fifth character,
search for
food and feed alone,
is difficult to define precisely
because chicks of many species find their own food
but remain in family groups. Furthermore, other as-
pects of parental care, including protection and brood-
ing, are not included in the precocial characters but
may be equally indicative of developmental state.
Whereas precocial birds are characterized by pat-
terns of behavior such as nest attendance, characters
six through nine describe altricial hatchlings accord-
ing to parent-chick interactions and developmental
traits (eyes closed at hatching, lacking external feath-
ers). Some of these are ambiguous and may even be
misleading. Character six,
young fed by the parents
,
(g)

can crow (
Corvus brachyrhynchos
) chicks hatch with
a dense cover of down, but black-billed magpie (
Pica
pica
) and carrion crow (
Corvus corone
) hatch naked.
Graded differences in the number of neoptiles, their
length, and the presence and absence of feather tracts
(pteryla) have been described for a large number of
passeriform families (Wetherbee 1957; Collins 1963,
1965, 1968; Arnold et al. 1983). Within Psittaciformes,
hatchlings of the Loriidae have a thick down cover but
parrots (Psittacidae) have only very little down or are
naked (Forshaw 1973). Such variability is not restricted
to the time of hatching. Skutch (1976) reports that the
blue-throated motmot
(Aspatha gularis)
, a species of
the high Guatemalan mountains, hatches naked but
soon develops a thick coat of down. The closely re-
lated turquoise-browed motmot
(Eumomota super-
ciliosa)
, which lives in tropical lowlands, does not
develop feathers until it is almost fully grown. Lack of
feathers at hatching is not specific for altricial birds:
in many altricial taxa, neonates have dense natal down,
whose function is not well understood.
We have reformulated the nine characters to make
the diagnostic features of each development class more
evident and uniform (Table 1.2). Four basic characters
are employed in classification systems, each with two
or more states, as follows: plumage (none, natal down,
or feathers), condition of eyes (closed or open), nest
attendance (stay, remain in area, or leave), and paren-
tal care (parental feeding, parental food-guiding, brood-
ing and protection only, or none). Even this arrange-
ment clearly combines interdependent developmental,
behavioral, and ecological traits. As with all such clas-
sification schemes, it is necessarily nonmetric and ar-
bitrary and only loosely tied to the developmental state
of the hatchling. Even the major split between the
altricial and precocial groups hinges on whether young
chicks spend time away from the nest site itself (semi-
precocial) rather than remaining in the nest (semialtri-
cial). This distinction may depend on the nest site as
much as on development. For example, the chicks of
cliff- and tree-nesting species tend not to wander from
the nest, even though they may be fairly mobile. Some
ground-nesting species, such as penguins, tend not to
leave the nest because of the dangers of wandering in
dense colonies.
For the most part, the arrangement in Table 1.2 de-
fines a one-dimensional ordering of developmental
types. In part, this results from the particular charac-
ters included, which were chosen to represent a se-
quence of developmental types. As pointed out, the
states of several of the characters are contingent on
the states of others, as chicks cannot leave the nest
unless their eyes are open and cannot be self-feeding
until they leave the nest. Other characters might not
be so consistently ordered. For example, thermal in-
dependence at an early age is well developed in some
semialtricial Procellariiformes (Ricklefs et al. 1980)
but relatively poorly developed in many precocial
shorebirds such as Scolopacidae (Visser and Ricklefs
1993; see chapter 5).
There are few apparent exceptions to the order of
characters in traditional classifications of the develop-
mental state of the neonate. The South American
hoatzin
(Opisthocomus hoazin)
is difficult to place
because it hatches sparsely covered with down, but its
eyes are wide open 24 hours after hatching. When two
weeks old and before they are feathered, chicks start
to clamber about on branches of their nesting trees
(Dominguez-Bello, personal communication). Under
normal conditions the chicks stay close to the nest,
which is always built in trees over the open water of
rivers. However, when predators approach they jump
out of the nest into the water, hiding among emergent
vegetation. Later, the chicks climb back into the nest.
Storm petrels (Hydrobatidae) and many of the petrels
(Procellariidae) provide another contrary example.
These hatch after long incubation periods densely cov-
ered with down, with their eyes soon open, and they
stay in the nest or burrow for long periods unattended
by their parents. Their thermogenic capacity (Farner
and Serventy 1959; Wheelwright and Boersma 1979;
Bech et al. 1982) and aspects of their internal anatomy
resemble those of many precocial species. Because of
the vagueness of the traditional classification they have
Table 1.2 Reorganization of diagnostic features of Nice’s developmental classes
Plumage Eyes Nest attendance Parental care
Precocial-1 Contour feathers None
Precocial-2 Leave Brooding
Precocial-3 Open Food showing
Precocial-4
Semiprecocial Down Nest area
Semialtricial-1 Parental feeding
Semialtricial-2 Closed Stay
Altricial None
8Avian Growth and Development

been placed as semialtricial by Nice (1962) and
O’Connor (1984) and as semiprecocial by Ricklefs et
al. (1980) and J.M.Starck (1993). Hatchlings of loons
and grebes (precocial-4) can swim ably but are often
carried and fed by their parents. It is hard to believe,
however, that they are less developed than waders (pre-
cocial-2) and phasianids (precocial-3). The difference
in behavior seems to be related to food supply and
habitat rather than to development. Among altricial
birds, we find species that are similarily difficult to
place in the traditional altricial-precocial classification.
For example, many pigeons and doves (Columbidae),
although highly altricial when hatching, leave the nest
when only half grown (
Geopelia cuneata
;
Oena
capensis
) and in the case of the purple-crowned fruit
pigeon (
Ptilinopus superbus)
as little as one-quarter
grown (Crome 1975).
Developmental patterns appear to be conservative
and are generally uniform within large taxonomic
groups. Auks (Alcidae) are probably the most diverse
family in modes of development. Most species are clas-
sified as semiprecocial, but guillemots (
Cepphus
spp.),
auklets (
Aethia
spp.,
Cyclorhynchus
spp., and
Cerorhinca
spp.), and puffins (
Fratercula
spp.) leave
the nest at 40 – 60 days of age, at 75% to 100% adult
body mass, after which they are independent of their
parents. Chicks of common murre (
Uria aalge
), thick-
billed murre (
U. lomvia
), and razorbill (
Alca torda
)
leave the nest after 20 – 30 days when they have
reached about 25% adult size. Because the chicks are
fed for some time after they leave the colony, they are
described as intermediate between semiprecocial and
precocial-4 (Sealy 1973; Gaston 1985). True precoc-
ity is found among the murrelets (
Synthliboramphus
spp.;
Brachyrhamphus
spp.) whose chicks leave the
nest (Gaston 1992) soon after hatching and are cared
for by their father during posthatching development
(precocial-4). However, the distinction among semipre-
cocial, intermediate, and precocial-4 behavior in auks
is exclusively based on the fledging time, nest attend-
ance, and relative size of the fledglings. Such differ-
ences in time of fledging are related more to the feed-
ing ecology (e.g., in-shore versus off-shore feeders)
of the species (Ydenberg 1989) than to developmental
differences. We discuss later a developmental scaling
of avian neonates, which shows that auks are placed
well within the precocial range.
The families within the order Charadriiformes,
which includes the Alcidae, are the most diverse in
development. Species range from the precocial-2
shorebirds (Scolopacidae and Charadriidae) to the
semiprecocial Laridae and semialtricial Dromadidae.
How much the neonates of these groups differ in physi-
ological and developmental advancement is not well
understood.
9Patterns of Development: The Altricial-Precocial Spectrum
1.3. 1.3.
1.3. 1.3.
1.3. TT
TT
The he
he he
he AltrAltr
AltrAltr
Altricial-Pricial-Pr
icial-Pricial-Pr
icial-Precocial Spectrecocial Spectr
ecocial Spectrecocial Spectr
ecocial Spectrumum
umum
um
and and
and and
and AA
AA
Avian Systemavian Systema
vian Systemavian Systema
vian Systematicstics
ticstics
tics
To study the evolutionary history of a clade, one would
ideally like to place character states on a true phylogeny
of the groups. This mapping would indicate ancestral
and derived characters, reversals, and convergences.
One of the ambiguities of this approach is that the dis-
tribution of character states among taxa provides the
basis for estimating phylogenetic relationships by us-
ing both cladistic and phenetic methods. Thus, the
character of interest may actually contribute to build-
ing the phylogeny that will be used to interpret its evo-
lution. One way to circumvent this problem of circu-
larity is to base the phylogeny on traits other than the
one of concern.
Early classifications and systematic arrangements
of birds used the developmental state of the hatchling
as a basic character to distinguish groups at high taxo-
nomic rank. Following von Baer (1828), most nine-
teenth-century avian biologists believed that develop-
ment was evolutionarily conservative, and they used
development as a taxonomic character for higher lev-
els of classification. This resulted in placing species
with similar developmental patterns together, reinforc-
ing in our collective conscience the idea of evolution-
ary conservatism. This practice reflected certain pre-
sumptions about the evolution of developmental grade
that persist to the present. Here we inquire about the
distribution of the developmental mode with respect
to more recent phylogenies based on molecular infor-
mation or on the analysis of morphological data. When
viewed in the light of these new phylogenetic classifi-
cations, is the developmental pattern evolutionarily
conservative or flexible?
Lorenz Oken (1779 – 1851), who was professor of
natural history at the University of Jena in Germany,
introduced the terms
Nestflüchter
(“nidifugous”) and
Nesthocker
(“nidicolous”) into scientific discourse
(Oken 1837). He based his classification of birds on
the distinction between nidifugous and nidicolous
development. His system was typically pre-Darwin-
ian and attempted to arrange bird taxa according to a
hierarchical rank in parallel to a classification of other
classes of vertebrates.8 In his system, nidifugous birds,
especially Galliformes, were ranked high because do-
mesticated species are useful to humans; songbirds
were ranked low because they are not. Although Oken’s
classification was soon replaced by others, the deve-
lopmental state of the hatchling (that is, altricial ver-
8 For example, the taxon “nidifugous birds” was subdivided
into four tribes, in parallel to the classes of vertebrates: (1)
fishlike birds = all swimming and diving birds with short legs;
(2) amphibianlike birds = wading birds with long bills; (3)
perfect birds = Galliformes; (4) mammal-like birds = walking
birds with strong legs but mostly missing the fourth toe.

sus precocial) remained an important character in the
classification of birds. Sundeval (1836, 1872) also
based his classification of birds on the ontogenetic
mode. He introduced the terms
Altrices
and
Precoces,
which referred more to parental feeding versus self-
feeding than to nest attendance by the chick. Sundeval’s
(1872) publication was translated into English by
Nicholson (1889), whereby it gained some importance
among English-speaking scientists. The English orni-
thologist Newman (1850) had previously used the
terms
hestogenous
for precocial and
gymnogenous
9
for altricial and had split the class of birds into two
subclasses characterized either by precocial or altricial
development. Bonaparte (1853) distinguished two sub-
classes of birds, the
Precoces
(Grallatores)10 and the
Altrices
(Insessores).11 Fitzinger (1856) established
five equivalent groups (“rows” in his terminology) of
birds,
Dickfüßige Aetzvögel
(thick-footed birds that
feed their young),
Dünnfüßige Aetzvögel
(thin-footed
birds that feed their young),
Scharrvögel
(scratching
birds, i.e., terrestrial birds),
Wadvögel
(wading birds),
and
Schwimmvögel
(swimming birds), thus contrast-
ing two altricial classes with three classes of birds that
were defined by their locomotion. Haeckel (1866) also
retained a basic separation of birds on the supraordinal
level into nidifuges (Autophagae,12 Nidifugae, and
Nestflüchter) and nidicoles (Paedotrophae,13 Inses-
sores, and Nesthocker). Lilljeborg (1866) based his
systematic review of the class of birds on Sundeval’s
classification. However, the distinction between
altricial and precocial birds appears in his description
of orders but is not used as a major character for clas-
sifying birds.
Shortly after the appearance of Darwin’s
On the
Origin of Species
in 1859, several classifications of
birds were elaborated strictly on the basis of morpho-
logical similarities. The papers by Huxley (1867),
Fürbringer (1888), and Gadow (1891, 1893) are out-
standing examples of modern classifications of birds,
based on morphological data acquisition and the prin-
ciple of evolution. Fürbringer (1888) used a technique
to reconstruct phylogeny that is similar to the cladistic
approach developed by Willi Hennig (1950) 75 years
later. It is important to note, however, that Gadow inclu-
ded developmental mode as a trait for the basic sepa-
ration of avian orders: “Nestflüchter” (nidifugous birds,
i.e., Galliformes, Charadriiformes, and Gruiformes),
“niedere Nesthocker” (lower nidicolous birds, i.e.,
Sphenisciformes, Procellariformes, and Ciconiifor-
mes), and “höhere Nesthocker” (higher nidicolous
birds, i.e., Columbiformes, Accipitriformes, Psittaci-
formes, Piciformes, and Passeriformes). Mode of de-
velopment is listed as the first trait in his extensive
character tables for classification of birds (pp. 69 –
92). Gadow described nidifugous development as an-
cestral, whereas nidicolous birds were separated into
two equally ranking groups of “Niedere Nesthocker”
and “Höhere Nesthocker.” He thought the two groups
of nidicolous birds had evolved independently.
Later, Wetmore (1930, 1934) adopted Gadow’s
(1893) arrangement of the nonpasseriform orders in
his systematic classification of the birds of the world
(Bock 1990), which ultimately provided the basis for
the linear arrangement of birds in Peters’s
Check-list
of the Birds of the World
(1937 – 1987). Stresemann
(1927 – 1934) also refers to Fürbringer, Gadow, and
Wetmore in his attempt at a classification of birds.
However, Stresemann’s pessimistic view about know-
ing avian phylogeny led him to develop a classifica-
tion with a larger series of orders of equal rank. Al-
though his linear arrangement of orders implies some
evolutionary development, he explicitly avoided state-
ments about the phylogenetic relationships between
the orders. His description of orders and families re-
fers to the developmental stage of the hatchling, in a
manner comparable to that of Liljeborg (1866), but
Stresemann did not use this trait as a diagnostic char-
acter. However, even without phylogenetic implica-
tions, he believed precocial development to be ances-
tral among birds and altricial chicks as derived. Mayr
and Amadon (1951) in their classification of extant
birds also retain Wetmore’s original sequence of non-
passeriform birds.
1.3.1. Recent ph1.3.1. Recent ph
1.3.1. Recent ph1.3.1. Recent ph
1.3.1. Recent phyloylo
yloylo
ylogg
gg
geniesenies
eniesenies
enies
Two recent avian classifications have been constructed
by using current phylogenetic methods. Cracraft (1981,
1986, 1988) applied cladistic methods to morphologi-
cal (skeletal) characters in an analysis of avian orders,
including extinct groups known only from fossils.
Sibley and Ahlquist (1990) used phenetic (distance)
analysis of DNA-DNA hybridization data to produce
a phylogeny of all major taxa of the birds of the world,
down to the taxonomic levels of genus and species in
many cases. These classifications are based on totally
different methods and data, and neither refers to de-
velopmental characters of hatchlings. Because all pre-
vious classifications at least implicitly refer to the mode
of development, only Cracraft’s and Sibley and Ahl-
quist’s phylogenies are suitable for post hoc descrip-
tions of the evolution of avian developmental patterns.
9
Hesto-
: from the Greek εστηµα, “garment”;
gymno-
: from
the Greek (γυµνοσ, “naked”;
-genous
: from the Greek
γεννοµαι, “being born.”
10
Grallatores
:
from the Latin
grallator
, “a person walking on
stilts.”
11
In-:
from the Latin
in
, “within”;
-sessores
:
from the Latin
sedere
, “sit.”
12
Auto-
: from the Greek αυτοσ, “self”;
-phagae
: from the
Greek ϕαγειν, “feed.”
13
Paedo-
: from the Greek παισ, “child”;
-trophae
: from the
Greek τρεφω, “nourish.”
10 Avian Growth and Development

11Patterns of Development: The Altricial-Precocial Spectrum
14 Cracraft does not explain why he did not consider Psitta-
ciformes, Cuculiformes, Trogoniformes, and Coliiformes in
the analysis.
We consider both phylogenies in parallel and discuss
their contrasting implications. To determine whether
altricial or precocial development was the ancestral
state in birds, we also examine development in poten-
tial outgroups (i.e., crocodiles as an extant outgroup
within archosaurs and dinosaurs as a fossil stem group).
Cracraft’s (1981, 1988) phylogeny is based on mor-
phological (skeletal) characters and attempts to resolve
the major clades of birds. Although the phylogeny con-
tains several unresolved polytomies (i.e., several clades
branch off from the same node, resulting in a phylo-
genetic bush rather than a dichotomously branching
tree), it presently is the only phylogenetic hypothesis
of any consequence that concerns the relationships
among orders of birds. Exclusively precocial develop-
ment appears only in the Palaeognathae (Struthioni-
formes in other classifications), the Galliformes, the
Anseriformes, the Podicipediformes, and the Gavii-
formes (Fig. 1.2). Altricial development is found
among many of the higher taxa. Cracraft’s cladogram
suggests that precocity is an ancestral character for
birds. However, the unresolved polytomies do not al-
low for a single interpretation. We may assume that
precocial development is ancestral for the higher taxa
of birds and that altriciality, including semialtricial-2
and altricial in Nice’s (1962) sense, evolved at least
six times independently in different clades (Sphenisci-
formes; Pelecaniformes and Procellariiformes; Colum-
biformes; Passeriformes, Piciformes and Coraciifor-
mes; Apodiformes and Caprimulgiformes; Strigifor-
mes).14 Alternatively, we may assume that altriciality
evolved in the stem group of all higher taxa of birds
and that precocity in loons and grebes, as well as in
cranes and waders, represents a reversal of that char-
acter. Also, semialtricial development in herons, storks,
and raptors would be reversals from the altricial deve-
lopment toward more precocial development. Both
alternatives assume six independent evolutionary
events and are equally parsimonious. Cracraft’s phy-
logeny suggests precocial development as the ances-
tral character for birds but does not clarify the evolu-
tion of the developmental mode in the higher taxa.
Multiple evolutionary origins of altriciality, as well as
reversal from altricial to precocial, may be inferred
equally from his cladogram.
Sibley and Ahlquist’s (1990) phylogeny of birds
arranges all exclusively precocial orders in the infra-
class Eoaves (Fig. 1.3). The button quails, which
emerge from the first basal node as a sister group to
the Neoaves, are also precocial.15 Button quails are
assigned the rank of an (unnamed) infraclass with one
order
incerte sedis.16
All orders of the Neoaves except
the Gruiformes and Ciconiiformes comprise taxa with
altricial development. Thus, Sibley and Ahlquist’s phy-
logeny suggests that precocial development is ances-
tral for birds, provided that the button quails are placed
correctly. When the button quails are not included in
the phylogeny, it is not possible to decide whether the
altricial or precocial development is the derived char-
acter state for birds, unless the presumed sauropsid
stem group of birds was known to be precocial. Within
the Neoaves, however, altriciality is almost certainly
the ancestral character. Precocity evolved as a derived
trait from altricial stem groups within the Gruiformes
and the Ciconiiformes. The Ciconiiformes, according
to Sibley and Ahlquist, are a most diverse group, em-
bracing 29 families, and are hardly comparable to the
Ciconiiformes of most traditional classifications (e.g.,
Morony et al. 1975). If we assume altriciality in the
stem group of Ciconiiformes and Gruiformes, precoc-
ity must have independently evolved at least four times:
in the order Gruiformes, in the suborder Charadrii, in
grebes (Podicipedidae) within the parvorder Podici-
pedida, and in the loons (Gaviidae) within the parvorder
Sulida. Altriciality, including semialtriciality, in all
other taxa of the Ciconiiformes is considered a plesio-
morphic (phylogenetically ancestral) character.
Both the Cracraft (1981, 1988) and the Sibley and
Ahlquist (1990) phylogenies are somewhat ambigu-
ous in what they tell us about the evolution of the
altricial-precocial spectrum. Cracraft’s cladogram in-
dicates precocial development at the base of all birds
and either several independent origins of altriciality or
altriciality at the base of all higher taxa but several
independent reversals back to precocial development.
Sibley and Ahlquist’s hypothesis is ambiguous about
whether the altricial or precocial mode of development
was ancestral in birds, depending on whether one con-
siders the Turniciformes as correctly placed.17 How-
15 The taxon Eoaves in Sibley and Ahlquist’s (1990) phylogeny
embraces Craciformes, Galliformes, and Anseriformes together
with the Tinamiformes and Struthioniformes in Fig. 353 (p.
838). The Eoaves are the sister taxon to Turnicimorphae and
Neoaves (including all other birds). However, the DNA-DNA
hybridization has a weak resolution at high taxonomic level,
failing to produce 50% single-stranded DNA for any
comparison of paleognathous birds with other birds. Therefore,
the phylogenetic branching pattern is based on extrapolated
∆T50H values. The Sibley and Monroe (1990) classification
deviates from the phylogeny and includes Galloanseres and
Turniciformes into the Neoaves without further explanation.
We use the original branching into Eoaves and Neoaves
throughout our analyses. However, the poor resolution of the
basal nodes in this study must be kept in mind for any
interpretation that is based on this phylogeny.
16
Incerte sedis
refers to an uncertain phylogenetic relationship.
17 Traditionally, Turnicidae were placed either as a family in the
Galliformes or in the Gruiformes (Peters 1934). Recent evidence
supports a phylogenetic relationship of Turnicidae and Rallidae,
that is, Gruiformes (Starck and Rotthowe 1996).

12 Avian Growth and Development
FF
FF
Figig
igig
ig. 1.3. . 1.3.
. 1.3. . 1.3.
. 1.3. Cladogram of the orders of birds (from Sibley and Ahlquist 1990). Slashed lines indicate precocial taxa; single-lined
clades comprise altricial taxa.
FF
FF
Figig
igig
ig. 1.2. . 1.2.
. 1.2. . 1.2.
. 1.2. Cladogram of the orders of birds (from Cracraft 1988). Slashed lines indicate precocial taxa; single-lined clades
comprise altricial taxa.

precocially while the ornithischian
Maiasaura peeple-
sorum
developed altricially. They thought that
Maiasaura
might have stayed in the nest until one-
quarter grown. Weishampel and Horner (1994) used a
cladogram to analyze the evolution of life histories of
dinosaurs, with special reference to the mode of de-
velopment. The admittedly incomplete data suggest
altriciality in Hadrosauridae (
Telmatosaurus
,
Maia-
saura
, and an undescribed
Hypacrosaurus
). Jacobs et
al. (1994) described the young of nodosaurids (Ornithi-
schia) and suggested that they exhibited altricial deve-
lopment based on the incomplete development of the
epiphyses of their long bones. Altricial development
also was assigned to an embryo or hatchling of
Cam-
ptosaurus,
which had not yet ossified epiphyses (Chure
et al. 1994). Winkler and Murry (1989) described ac-
cumulations of juvenile hypsilophodontid dinosaur
bones (species not determined) of different size classes,
which they interpreted as representing nests with young
of different ages. Similar dinosaur nests were also de-
scribed by Horner and Makela (1979) and Horner
(1982, 1988, 1996), suggesting that altriciality, ex-
tended nestling periods, and possibly parental care may
have been characteristic of some dinosaur species. This
view has recently been challenged by Geist and Jones
(1996), who found that the state of fossilization of long
bone epiphyses is not indicative of mode of develop-
ment.
The closest extant relatives of birds among the
archosaurs are crocodiles, even though crocodiles and
birds have evolved on separate phylogenetic lineages
for at least 200 million years. Parent crocodiles care
intensely for their brood in various ways, but the
hatchlings are clearly precocial. Because precocity is
found in both crocodiles and basal avian taxa (Eoaves),
we cannot determine whether precocial development
is ancestral or secondarily and independently derived.
In conclusion, neither the fossil record of embryonic
archosaurs nor the closest living relatives of birds tell
us much about the ancestral developmental mode in
birds. There is some evidence, however scarce and
ambiguous, that altriciality might have evolved in di-
nosaurs, but the developmental mode of the stem group
of birds is still unknown. Regardless of whether pre-
cocity or altriciality was the ancestral state, the other
would have to have evolved independently in at least
two lineages.
13Patterns of Development: The Altricial-Precocial Spectrum
ever, their phylogeny leaves little doubt that altriciality
is a derived character of the Neoaves (or higher taxa
of birds) and that precocity arose secondarily and in-
dependently in several taxa. One way to resolve un-
certainty about the basal condition of birds and to help
understand the phylogeny of developmental patterns
is to study the living and fossil representatives of
sauropsid outgroups and stem groups.
1.4. 1.4.
1.4. 1.4.
1.4. TT
TT
The Fhe F
he Fhe F
he Fossil Recorossil Recor
ossil Recorossil Recor
ossil Record of thed of the
d of thed of the
d of the
AltrAltr
AltrAltr
Altricial-Pricial-Pr
icial-Pricial-Pr
icial-Precocial Spectrecocial Spectr
ecocial Spectrecocial Spectr
ecocial Spectrumum
umum
um
Rare findings of fossilized embryonic skeletons of
birds have provided some insight into the ancestral state
of the mode of avian development. Based on embry-
onic bird skeletons from the late Cretaceous of Mon-
golia, Elzanowski (1981, 1983, 1995) suggested that
the young of
Gobipteryx minuta
were superprecocial.
His ideas were based on the degree of ossification of
the skeletal remains of embryonic
Gobipteryx
. He rea-
soned that the large extent of ossified areas in the
appendicular skeleton indicated capability of flight, and
thus superprecocity. In another paper, Elzanowski
(1985) argued that hypothesized limitations on the
ability of parent birds to feed their chicks supported
his idea of superprecocity as the ancestral mode of
development in birds. He also argued in circular fash-
ion that superprecocity can be deduced from skeletal
findings, from which he infers that the
Gobipteryx
laid
extremely large eggs, suggesting extremely long lay-
ing intervals, which do not allow for parental care, thus
suggesting superprecocity. Furthermore, the Enanthior-
nithes seem to represent an early Cretaceous radiation
of birds, with
Gobipteryx
as a derived offshoot with-
out close relationship to the stem group of modern birds
(Feduccia 1995). Recently, Chatterjee et al. (n.d.) de-
scribed embryonic skeletons of
Gobipipus reshetovi,
a ducklike bird from the Upper Cretaceous of the Gobi
desert. Chatterjee et al. pursued arguments similar to
those of Elzanowski in his earlier papers, but consid-
ered the degree of ossification of the skeletal remains
of
Gobipipus
as indicating precocial rather than
superprecocial development. As we see in chapter 3,
however, the degree of ossification is a poor predictor
of developmental mode. Thus, no indication of whether
the stem group of birds was altricial or precocial comes
from fossil embryonic birds.
Horner and Weishampel (1988) briefly reported on
embryonic skeletons of an ornithischian and a theropod
dinosaur. On the basis of fine-structural analyses of
the epiphyses of leg bones, they claimed that the
theropod dinosaur
Troodon cf. formosus18
developed
1.5. 1.5.
1.5. 1.5.
1.5. A NeA Ne
A NeA Ne
A New Metrw Metr
w Metrw Metr
w Metric fic f
ic fic f
ic for or
or or
or AA
AA
Avian Havian Ha
vian Havian Ha
vian Hatctc
tctc
tchlings?hlings?
hlings?hlings?
hlings?
In most classifications of avian development, many
intermediate forms, or grades, are spread between the
two extremes of the altricial and precocial conditions.
To understand better the evolution of the developmen-
tal pattern, it would be helpful to know whether devel-
opmental grades are distributed along one or more di-
mensions of variation, whether species tend to be
18 The original publication erroneously described that specimen
as
Oreodromeus makelai.
Its true identity has just recently been
described after further preparation (Horner and Weishampel
1996).

quired by different environmental settings and levels
of parental care.
We use the dry matter content of a tissue as an in-
dex to its functional maturity. Dry matter content ap-
pears to be generally associated with the working ma-
chinery of cells and connective tissues. We assume
that this is a general phenomenon among birds, if not
vertebrates, which makes dry matter content directly
comparable among all species. It increases with age
in virtually all tissues and all species, both before and
after hatching (Ricklefs 1983). Other measures of func-
tional maturity, such as the activities of certain en-
zymes, are often age- and tissue-specific and may vary
widely among species, as in the case of aerobic versus
glycolytic pathways of energy metabolism in species
with sustained versus burst-type activity. In addition,
changes in dry matter content of particular tissues usu-
ally are well correlated with changes in other meas-
ures of function, such as the activities of enzymes in
skeletal muscles over the course of maturation of those
tissues (Marsh and Wickler 1982; Choi et al. 1993).
Finally, dry matter content of tissues is inversely cor-
related with growth rates, reflecting the generally in-
verse relationship between embryonic activity and
functional maturity (Choi et al. 1993; Ricklefs et al.
1994). Thus, dry matter content links the functional
capacity of the neonate to other aspects of growth that
have a direct bearing on evolutionary fitness.
Tissues that begin to function at different times
during development might exhibit different rates of
maturation. For example, the neonatal gut must digest
food and assimilate nutrients in all species, the stom-
ach and liver are probably equally employed in both
altricial and precocial neonates, and cardiac muscle
also is functional in all species prior to hatching; thus,
one would not expect to find consistent differences in
the water contents of these tissues at hatching
(O’Connor 1977, 1978a, 1978b). In contrast, skeletal
muscles used for flight and pedal locomotion develop
at different times and come into use at different times
in different species, depending on when the chick
leaves the nest and when it begins to fly. For example,
ducks walk and swim virtually from hatching but do
not fly until the end of the growth period; galliform
chicks achieve flight when they are still smaller than
adults. Some parts of the brain must function in all
species from an early age to accomplish certain sim-
ple behaviors. Even altricial neonates respond to
stimuli that indicate the presence of adults, and they
can solicit food; altricial neonates also can sense brain
temperature and engage behavioral mechanisms to
dissipate heat to regulate body temperature even if they
cannot generate heat metabolically for this purpose.
However, more complex behaviors and locomotion
develop at different times in different species and place
different requirements on the development of function
in the higher centers of the brain.
clumped into distinct groups or are continuously dis-
tributed along the developmental gradient(s), or
whether gaps separate the distributions of major de-
velopmental grades. The presence of clusters of spe-
cies would suggest discrete developmental strategies
that rest on adaptive peaks, particularly if each cluster
included species from more than one lineage. The pres-
ence of gaps in an otherwise continuous distribution
would suggest that intermediates are not viable deve-
lopmental possibilities: neither precocial enough to
function independently nor altricial enough to reap
fully the benefits of intensive parental care.
Any new scaling of a neonatal condition, of course,
can be compared to the classical altricial-precocial
spectrum. However, whether a new scaling can, or
should, replace an older classification system is a dif-
ficult question. The answer to this question depends
on why we wish to classify developmental patterns
and on the particular context and goals we have for
clarifying strategies of growth and development. For
example, Portmann’s (1935 – 1962) studies on the evo-
lution of development in birds and mammals were
guided by the idea of a graded hierarchy of increasing
integration of morphology, physiology, and behavioral
traits. His goal was to establish a hierarchical system
of “morphogrades,” with the most complex forms on
top of the hierarchy. In contrast to that approach, Nice
(1962) attempted to develop a classification system of
bird hatchlings suitable for comparative behavioral
studies. For example, the distinction between semi-
altricial and semiprecocial, basically whether the chick
leaves the nest site or remains at the nest, may have
less to do with the developmental state of the neonate
than it does with the structure and placement of the
nest and with the chick’s behavior in the nest-site con-
text. Thus, depending on the purpose of the classifica-
tion, this distinction may be useful or confusing. Our
goal is to understand the evolutionary pathways of
ontogenetic development. For this purpose, a system
that distinguishes development patterns by functional
(physiological) measures that are strictly comparable
across taxa will be most useful.
Here we develop a continuous metric to describe
the state of maturation of the neonate. We use this
metric to examine the relationship of traditional clas-
sifications to a scale of development with clear func-
tional meaning, and we apply this scale to understand
the evolutionary diversification of patterns of devel-
opment among the clades of birds. We chose a meas-
ure of functional capacity at the tissue level, rather than
an organism-level criterion, to focus on maturation of
function and avoid the complication of environment-
dependent behavior. The functional maturity of tissues
can be compared directly across species independently
of the chick’s surroundings. Furthermore, functional
maturity may determine the potential capacity of the
neonate for a wide variety of different behaviors re-
14 Avian Growth and Development

1 10 100
0.05
0.07
0.09
0.2
0.3
Neonate mass (MN)
1 10 100
0.2
0.3
0.1
Lean dry fraction (LDF)
0.2
0.3
Lean dry fraction (LDF)
0.06
0.08
0.15
0.1
1 10 100
0.2
0.3
0.4
0.1
Neonate mass (MN)
1 10 100
0.06
0.08
0.1
Brain Heart
Liver Leg muscle
Stomach Pectoralis muscle
FF
FF
Figig
igig
ig. 1.4.. 1.4.
. 1.4.. 1.4.
. 1.4. Relationship of lean dry fraction of tissues and neonate mass for six different organs (brain, heart, liver, leg muscle,
stomach, and pectoralis muscle). Mode of development is indicated by the following labels: open circles, altricial neonates;
open triangle, semialtricial neonates; solid triangle, semiprecocial; solid circle, precocial. The same labels for mode of devel-
opment are used in all figures of this chapter.
Analysis of the dry matter contents of several tis-
sues across species will reveal one or more dimen-
sions of variation, depending on the degree to which
the dry matter contents of the different tissues vary
independently among species. If variation is multidi-
mensional, one could conjecture that the course of
maturation of each tissue responded independently of
others, depending on the particular requirement of the
chick. In contrast, if the dry matter contents of differ-
ent tissues vary in parallel, each tissue would appear
to gain its functional maturity on the same developmen-
tal schedule, whether its functional capacity is used or
15Patterns of Development: The Altricial-Precocial Spectrum

log10 neonate mass
0.5 1.0 1.5 2.0
log10 LDF
-0.8
-0.6
-0.4
not. Hypothetically, such unidimensional variation in
development might be dictated by some internal con-
straint of the developmental program, for example, the
response of tissue maturation to a common hormonal
environment. A single dominant dimension to varia-
tion in development also could reflect the similar tim-
ing of the functional development of each tissue as a
way of regulating the growth rates of tissues at about
the same level at a particular stage of development.
With a continuous scale of functional maturity (e.g.,
dry matter content) entered into a multivariate analy-
sis, we can address four issues: (a) the dimensionality
of variation in the development pattern, (b) the pattern
of distribution of species along axes of variation in
development, (c) the relationship of functional capac-
ity to traditional classifications of the developmental
state of the neonate, and (d) the evolutionary diversifi-
cation of the developmental pattern.
We assembled a data set for this analysis made up
of lean dry fractions (LDF, lipid-free dry mass/lipid-
free wet mass) of six tissues of the neonates of 46 spe-
cies of birds: the tissues were heart, pectoral muscle,
leg muscle, brain, stomach, and liver (Fig. 1.4). We
placed the 46 species in 14 taxonomic groups, follow-
ing Sibley and Ahlquist (1990), for further analysis of
between-group and within-group variation. These
groups are quail (Galliformes, 2 species); ducks (Anat-
idae, 9); geese (Anseridae, 1); coots (Rallidae, 1); sand-
pipers (Scolopacidae, 5); plovers (Charadriidae, 2);
gulls, terns, and skuas (Laridae, 12); alcids (Alcidae,
4); grebes (Podicipedidae, 1); tropic birds (Phaethont-
idae, 1); penguins (Spheniscidae, 1); petrels (Procellari-
iformes, 5); and songbirds (Passeriformes, 2).
In five of the six tissues, lean dry fraction decreased
with increasing mass of the neonate (
MN
) (Fig. 1.4).
Therefore, we calculated the residual of each value
from the equation relating lean dry fraction of tissue
to the logarithm of neonate mass. This was done by
analysis of covariance, in which taxonomic groups
were effects and the log10(
MN
) was the covariate. Thus,
the slope of the line relating lean dry fraction to
log10(
MN
) was the within-group regression. Both taxo-
nomic group and neonate mass had significant effects
on lean dry fraction for all tissues except liver, for which
neither group nor neonatal mass was significant. For
each tissue, a single regression line having the within-
group slope was established and forced through the
mean of the lean dry fraction of the tissue and the
log10(
MN
) of the entire sample. The slope of the rela-
tionship between the LDF and log10(
MN
) was highest
for the leg muscle (–0.064 ± 0.001 SE, that is, a de-
crease of 6.4% for each tenfold increase in neonate
mass); the slope varied between –0.020 and –0.034
for the pectoral muscle, stomach, and brain (Fig. 1.4).
The functional maturity of the neonate presents two
phenomena: a general decrease in dry matter content
of each tissue with increasing neonatal mass (Fig. 1.5)
and significant differences in the lean dry mass be-
tween taxonomic groups. The residuals of lean dry frac-
tion of each tissue with respect to body mass were
subjected to a principal components analysis based on
the correlation matrix, which normalizes the variation
of each of the variables (tissues) to the same standard
deviation (Fig. 1.6). The first principal component ex-
plained 70% of the total variance in the data set (Table
1.3). Variation in five of the six tissues (heart, pectoral
and leg muscles, brain, and stomach) contributed nearly
equally to the first component, reflecting the strong
correlations of the dry fractions of these tissues among
themselves (
r
= 0.66 to 0.87). The second principal
component uniquely comprises variation in the lean
dry fraction of the liver (Table 1.3).
The prominence of the first principal component
suggests that functional maturity might be conveniently
scaled on a single dimension. The high correlation of
the LDF values among most of the tissues further sug-
gests that the lean dry fraction of the entire neonate
might be a suitable measure of developmental grade.
Total lean dry fraction of the neonate is strongly cor-
related with the lean dry fraction of each tissue (
r
=
0.80 to 0.93) except liver (
r
= 0.61), and it is also re-
lated to the first principal component from the tissue-
level analysis (
r
= 0.85). Furthermore, differences be-
tween taxonomic groups explain more of the variation
in whole-body lean dry fraction (
R²
= 0.77;
F
13,32 =
8.2;
P
< 0.0001) than in the first principal component
(R²
= 0.68;
F
11,29 = 5.7;
P
< 0.0001). The values of
LDF of the neonate for individual species range from
a low value of 0.113 for the blue-eyed shag (
Phalacro-
corax auritus
), which is altricial in Nice’s (1962) clas-
sification, to a high of 0.340 for the blue-winged teal
(
Anas discors
), which is precocial-2. The LDF appears
to increase with the functional maturity (precocity) of
the neonate.
FF
FF
Figig
igig
ig. 1.5.. 1.5.
. 1.5.. 1.5.
. 1.5. Relationship of log10-transformed lean dry fraction
of neonates and log10-tranformed neonate mass. Regression
line was forced through the mean of
MN
.
16 Avian Growth and Development

Frequency
2
4
6
8
10
LDF
Principal component 1
-6-4-20246
PC2
0
FF
FF
Figig
igig
ig. 1.6.. 1.6.
. 1.6.. 1.6.
. 1.6. Principal component analysis of lean dry fractions
of neonates. For details of the analysis see text and Table 1.4.
for this index; –0.8 is approximately the intercept (at
neonate mass = 1g) for altricial species (e.g., Passerifor-
mes). Thus,
IP
is generally close to zero or positive,
with higher values indicating a higher dry matter con-
tent of a neonate of a given size (Figs. 1.6 and 1.7;
Table 1.4). The value of
IP
in our sample varies from –
0.18 for the house martin (
Delichon urbica
) to 0.44
for the brush turkeys
(Alectura lathami)
, indicating the
range among the species in our analysis. The 14 taxo-
nomic groups account for 91% (
R2
) of the total varia-
tion in
IP
(
F
13,32 = 24;
P
< 0.0001).
The distribution of species on the index
IP
reveals a
mixed pattern. On the one hand, the nonaltricial spe-
cies (semialtricial, semiprecocial, and precocial) are
spread out broadly along the upper part of the range of
values. If we consider only groups that are self-feed-
ing at hatching (precocials), these range from ducks
(
IP
= 0.37) to sandpipers (0.25), plovers (0.24), and
one galliform (0.16). Neonates of petrels (Procellari-
idae,
IP
= 0.24), alcids (Alcidae, 0.27), gulls, and terns
(Laridae, 0.24), which are downy but fed by their par-
ents (semialtricial or semiprecocial), fall within the
distribution of precocial species. The eared grebe (0.27)
and American coot (0.30), whose chicks are fed by
the parents during the early part of the postnatal pe-
riod but leave the nest soon after hatching (Nice’s pre-
cocial-4), are also well within the distribution of fully
precocial groups.
The second feature of the distribution of
IP
is a
substantial gap between most fully altricial species
(–0.18 – 0.04) and the semialtricial-2 Adelie penguin
(
Pygoscelis adeliae
, 0.14); a concentration of species,
both precocial and semiprecocial, in the range between
0.21 and 0.28; and the distribution of all the ducks and
the Canada goose (
Branta canadensis
) above 0.32.
Among the Procellariiformes, two species have an
IP
< 0.20, the southern giant fulmar (
Macronectes
giganteus
, 0.17) and the white-chinned petrel (
Procel-
laria aequinoctialis
, 0.196), whereas the other species
cluster between 0.26 and 0.29. The red-tailed tropic
bird (
Phaethon rubicaudis
) is at the low end of the
Table 1.3. Principal component scores of lean dry fraction of different organs (compare Fig. 1.6)
Eigenvectors
PC 1 PC 2 PC 3 PC 4 PC 5 PC 6
Brain 0.41 0.26 0.74 0.12 0.39 0.24
Leg 0.46 –0.11 –0.19 0.04 –0.85 –0.12
Heart 0.44 –0.24 0.51 0.06 0.25 –0.66
Liver 0.27 0.83 0.38 0.24 –0.06 0.17
Pectoralis 0.42 –0.41 0.07 0.49 0.20 0.61
Stomach 0.44 0.01 0.08 –0.83 0.13 0.32
Eigenvalue 4.18 0.91 0.39 0.27 0.15 0.10
Proportion 0.697 0.152 0.065 0.045 0.024 0.017
Cumulative 0.697 0.849 0.914 0.959 0.983 1.000
17Patterns of Development: The Altricial-Precocial Spectrum
The lean dry fraction of the neonate decreases with
the increasing mass of the neonate. An analysis of
covariance shows that the within-group regression of
the log10(LDF) on log10(
MN
) has a slope of –0.104
(0.019 SE;
R²
= 0.91;
F
14,31 = 22;
P
< 0.0001). Accord-
ingly, we define a normalized index of lean dry frac-
tion (
IP
) as the deviation from the allometric (log-log)
relationship of the lean dry fraction on neonate mass.
We suggest the equation
IP
= log10(LDF) – predicted log10(LDF) (1.1)
or
IP
= log10(LDF) + 0.1* log10(
MN
) + 0.8 (1.2)

Index of lean dry fraction (Ip)
-0.2
-0.1
0.0
0.1
0.2
0.3
0.4
0.5
altricialprecocial semi-
precocial semi-
altricial
12 3 4 12
Altricial
Precocial
2
3
8
4
46 1
22
23
44 50
7
49
48
55
54
53
36
43/51
30
27
24 28
59
60 57
58
26
21 25/56
61
13
10
16
15
37 31
17/4
18/45/47
19 9
11
6
12/14/20
34 38/41/42
29/32/35
33/40
39
52
5
Hatchling category (Nice 1962)
18 Avian Growth and Development
semiprecocial group (0.18), and the Japanese quail
(
Coturnix coturnix japonica
) resides at
IP
= 0.16.
Additional values for dry fraction have been re-
ported in the literature for neonates or term embryos
of several species, but the dry matter contents include
lipids (but not yolk) and are therefore somewhat in-
flated. These data nonetheless yield additional values
of
Ip
that reinforce the pattern presented previously. At
the precocial end of the spectrum, two species of mega-
podes exhibit high values (based on lipid-free masses)
of
IP
: mallee fowl (
Leipoa ocellata
) 0.40, and brush
turkey (
Alectura lathami
), 0.44 (Vleck et al. 1984).
Domesticated duck (0.31) and goose (0.34) also have
high
IP
values but perhaps lower than nondomesticated
species (Romanoff 1960). Additional data for galli-
forms, also from Romanoff, range between bobwhite
(
Colinus virginianus,
0.20), ring-necked pheasant
(
Phasianus colchicus,
0.39), domestic fowl (0.27), and
domestic turkey (0.31). Neonates of barred button quail
(
Turnix suscitator)
have surprisingly low values of
IP
,
averaging 0.125, possibly related to their extremely
small hatchling size. Values for altricial species include
indices of 0.01 for the altricial lovebird (
Agapornis
roseicollis,
Psittaciformes), –0.10 for zebra finch
(
Poephila guttata
, Passeriformes), –0.016 for the blue
tit
(Parus caruleus)
, –0.18 for the house martin
(Delichon urbica)
, and –0.10 for the house sparrow
(Passer domesticus)
. The brown pelican (
Pelecanus
occidentalis,
Pelecaniformes) is surprising at
IP
= 0.15,
considering that other Pelecaniformes, a booby and a
shag, have values of 0.04 and 0.01, respectively.
In several cases, variation in
IP
within groups ap-
pears to be related to differences in functional matu-
rity. For example, among the Procellariiformes, div-
ing petrels and fulmarine petrels (
IP
= 0.20, 0.17) are
brooded for several weeks after hatching and have a
weaker thermogeneric response to cooling than do
other petrels (
IP
= 0.26 – 0.29), which typically are not
brooded after hatching (Roby and Ricklefs 1983).
Values of
IP
for several species of “reptiles”19 were
at the lower end of the precocial range for birds or
even intermediate between altricial and precocial birds
(Ricklefs and Cullen, unpublished data): agamid liz-
19 Reptiles are a paraphyletic taxon of evolutionary classifi-
cation of vertebrates. For simplicity of reading we use “reptiles”
(in quotation marks), which is synonymous to the phyloge-
netically correct term
nonavian sauropsids.
FF
FF
Figig
igig
ig. 1.7.. 1.7.
. 1.7.. 1.7.
. 1.7. Correspondence between the index of lean dry fraction
(Ip)
of neonates and the hatchling categories of Nice (1962).
Numbers refer to species column in Table 1.4.

19Patterns of Development: The Altricial-Precocial Spectrum
Table 1.4. Neonatal mass (gram), dry matter fraction of the neonate based on lipid-free dry masses, index IP of
dry matter fraction of neonate mass as derived by the equation IP = log10(LDF) + 0.1 !" log10(MN) + 0.8, and
hatchling category according to Nice (1962). Numbers in species column refer to labels in Fig. 1.7.
Species Neonate mass (std.) LDF IPNice
1Turnix suscitator a 3.8 (0.439) 0.185 0.125 Precocial-4
2Alectura lathami b 87.2 0.281 0.443 Precocial-1
3Leipoa ocellata b89.4 0.254 0.400 Precocial-1
4Coturnix coturnix 5.8 (0.82) 0.192 0.160 Precocial-2
5Colinus virginianus c 6.12 0.211 0.203 Precocial-2
6Phasianus colchicus c 17.5 0.290 0.387 Precocial-2
7Gallus gallus f. dom. 0.27 Precocial-2
8Meleagris gallipavo f. dom. 0.31 Precocial-3
9Aythya valisineria 55.7 (5.69) 0.240 0.355 Precocial-2
10 Somateria molissimad43.1 (0.86) 0.269 0.393 Precocial-2
11 Somateria molissimae22.0 (0.76) 0.257 0.344 Precocial-2
12 Clangula hyemalis 26.6 (3.84) 0.249 0.339 Precocial-2
13 Anas discors 10.5 (0.75) 0.340 0.434 Precocial-2
14 Anas acuta 23.3 (1.03) 0.253 0.340 Precocial-2
15 Aythya americana 20.9 0.277 0.375 Precocial-2
16 Mergus cucullatus 24.7 (3.84) 0.307 0.426 Precocial-2
17 Anas platyrhynchos 18.5 (2.99) 0.246 0.318 Precocial-2
18 domestic duck 0.31 Precocial-2
19 Branta canadensis 59.6 (4.64) 0.241 0.360 Precocial-2
20 domestic goose 0.34 Precocial-2
21 Agapornis roseicollis f 2.6 0.148 0.012 Altricial
22 Podiceps nigricollis 9.3 (1.23) 0.235 0.268 Precocial-4
23 Fulica atra 10.0 (1.44) 0.252 0.301 Precocial-4
24 Pygoscelis adeliae 63.1 (4.58) 0.146 0.144 Semialtricial-2
25 Phalacrocorax auritus 33.7 (1.99) 0.113 0.006 Altricial
26 Sula sula 27.7 (2.34) 0.124 0.038 Altricial
27 Phaethon rubricauda 46.1 (5.15) 0.164 0.181 Semialtricial-2
28 Pelecanus occidentalis g 61.7 0.147 0.146 Altricial
29 Cepphus grylle 9.7 (0.19) 0.208 0.217 Semiprecocial
30 Aethia pusilla 58.9 (6.61) 0.221 0.321 Semiprecocial
31 Fratercula arctica 36.8 (7.41) 0.225 0.309 Semiprecocial
32 Uria aalge 21.4 (0.60) 0.194 0.221 Semiprecocial
33 Larus atricilla 51.5 (4.32) 0.200 0.272 Semiprecocial
34 Sterna hirundo 31.7 (5.24) 0.200 0.251 Semiprecocial
35 Rissa tridactyla 19.3 (2.76) 0.197 0.223 Semiprecocial
36 Catharacta skua 15.9 (2.19) 0.176 0.166 Semiprecocial
37 Sterna fuscata 26.0 (3.35) 0.222 0.288 Semiprecocial
38 Gygis alba 13.2 (1.31) 0.212 0.238 Semiprecocial
39 Larus philadelphia 12.4 (1.52) 0.226 0.264 Semiprecocial
40 Larus argentatus 41.9 (6.70) 0.204 0.272 Semiprecocial
41 Sterna paradisaea 16.4 (1.11) 0.219 0.262 Semiprecocial
42 Anous tenuirostris 21.3 (1.87) 0.204 0.243 Semiprecocial
43 Anous stolidus 8.5 (1.09) 0.202 0.198 Semiprecocial
44 Micropalma himantopus 6.1 (1.57) 0.215 0.211 Semiprecocial
45 Calidris minutilla 25.3 (1.37) 0.236 0.313 Precocial-2
continued

20 Avian Growth and Development
ard (
Amphibolurus barbatus,
0.09), snake (
Coluber
constrictor,
0.20), turtle (
Chrysemys picta,
0.21), and
iguana (
Iguana iguana,
0.11).
One point of correspondence between the scale of
functional maturity developed here and Nice’s (1962)
classification of neonates is the restriction of
IP
values
below 0.1 to the altricial species (Fig. 1.7). The preco-
cial ducks and megapodes occupy the extreme oppo-
site end of the scale, but other precocial groups, such
as the Galliformes and waders (Charadriidae and
Scolopacidae), are situated in the middle of the spec-
trum, along with the semialtricial petrels and penguins.
We find continuous variation in
IP
, with values for spe-
cies in several of Nice’s categories overlapping broadly.
Although variation in development mode within
orders and families is small compared to that between
orders and other higher taxa, the relationship between
functional maturity and phylogeny appears to be com-
plex (Fig. 1.8).
One may summarize the relationships
among the taxonomic groups by contrasting Sibley and
Ahlquist’s (1990) phylogeny, which is based on DNA-
DNA hybridization, with Cracraft’s (1986) phylogeny,
which is based on morphological characters. The ear-
liest major node, or branch point, separates the Eoaves,
which are all precocial in Nice’s (1962) terminology,
and the Neoaves, which encompass the whole range
of developmental types from precocial to altricial. Even
among the precocial Eoaves,
IP
appears to vary over
almost the full range of nonaltricial species, from the
ducks to the Galliformes. The basal taxa of the Neoaves
are altricial (Picae, Coraciae, Coliae, Cuculimorphae,
Psittacimorphae, and Apodimorphae). However, the
more derived taxa of the Gruiformes and Ciconiiformes
in our sample range from coots and grebes, which lie
close to the precocial end of the scale (0.30 and 0.27),
to shags and boobies (0.01 and 0.04), which cluster at
the altricial end. Thus, precocial (including semipre-
cocial) development has also been derived independ-
ently, at least in the Strigiformes (Caprimulgidae,
nighthawks with semiprecocial young) and in the
gruiform-ciconiiform lines. According to Sibley and
Ahlquist’s phylogeny, the evolution of secondarily
altricial development from nonaltricial ciconiiform
stem groups must have occurred in the Pelecanidae,
Sulidae, Anhingidae, and Phalacrocoracidae. In con-
trast, Cracraft’s phylogeny places all precocial forms
among the lower nodes of the cladogram. The results
of such comparisons are as conflicting as are the un-
derlying phylogenetic hypotheses, and it is difficult to
draw convincing conclusions based either on Sibley
and Ahlquist’s or Cracraft’s hypothesis.
Finally, we ask whether the level of functional ma-
turity (dry matter content) is related to other attributes
of the neonate associated with its functional capacity.
Natal down reduces the thermal conductance of the
neonate and is associated with endothermy. Down is
essentially absent in many altricial species, and so there
is a connection between natal down and
IP
at a large
Table 1.4 (continued)
Species Neonate mass (std.) LDF IPNice
46 Numenius phaeopus 2.3 (0.20) 0.202 0.142 Precocial-2
47 Phalaropus lobatus 4.6 (0.13) 0.281 0.315 Precocial-2
48 Calidris alpina 2.8 (0.07) 0.260 0.260 Precocial-2
49 Charadrius semipalmatus 12.3 (2.32) 0.232 0.275 Precocial-2
50 Pluvialis dominica 4.3 (0.28) 0.219 0.204 Precocial-2
51 Procellaria aequinoctialis 11.6 0.195 0.196 Semiprecocial
52 Oceanodroma leucorhoa 5.1 (0.81) 0.250 0.269 Semiprecocial
53 Pelecanoides urinatrix 94.0 (8.82) 0.196 0.290 Semialtricial-1
54 Pelecanoides georgicus 12.9 (1.53) 0.234 0.280 Semialtricial-1
55 Macronectes giganteus 85.3 (14.87) 0.149 0.166 Semialtricial-1
56 Aimophila carpalis 1.9 (0.35) 0.148 0.002 Altricial
57 Poephila guttata f0.6 0.134 0.095 Altricial
58 Parus caeruleus h1.2 (0.2) 0.150 0.016 Altricial
59 Delichon urbica h1.7 (0.2) 0.100 0.177 Altricial
60 Passer domesticus h3.5 (1.1) 0.110 0.104 Altricial
61 Sturnus vulgaris 8.7 (1.90) 0.134 0.021 Altricial
Data from a J.M. Starck (unpublished); b Vleck et al. 1984; c Romanoff (1960); d Greenland, probably S. m. borealis;
e Atlantic NE North America, probably S. m. dresseri; f Bucher et al. 1984; gBartholomew and Goldstein (1984).

21Patterns of Development: The Altricial-Precocial Spectrum
FF
FF
Figig
igig
ig. 1.8.. 1.8.
. 1.8.. 1.8.
. 1.8. Phylogenetic relationship of the species analyzed for index of lean dry fraction.

Index of lean dry fraction
-0.75-0.70-0.65-0.60
Dry mass of down as fraction of LDF
0.0
0.1
0.2
0.3
22
FF
FF
Figig
igig
ig. 1.9. . 1.9.
. 1.9. . 1.9.
. 1.9. Relationship between index of lean dry fraction
(IP)
and dry mass of down as a fraction of LDF.
of hatchlings. (e) Although species classified by Nice
as “altricial” fall within the first group, there seems to
be no clear distinction in functional maturity between
semialtricial, semiprecocial, and especially precocial
birds. Nice’s groups overlap considerably in functional
maturity (Fig. 1.7). (f) Putting the scale of functional
maturity next to Sibley and Alquist’s (1990) avian phy-
logeny suggests that although developmental maturity
exhibits taxonomic conservatism on the level of fami-
lies and orders, it appears to have shifted at several
evolutionary branch points that separate larger taxo-
nomic groups. Because the basal taxa of the Neoaves
are altricial, semiprecocial and precocial modes of
development in the Gruiformes and Ciconiiformes are
secondarily derived. Furthermore, the development of
boobies, shags, pelicans, and frigate birds may be sec-
ondarily altricial, having been derived from ancestral
taxa with nonaltricial development. Cracraft’s (1988)
phylogeny suggests even more independent evolution-
ary origins of altriciality. However, our general impres-
sion is that the mode of development is primarily a
quantitative variable, which may evolve rapidly across
the precocial to semialtricial range under suitable se-
lective pressures. It is apparently tied to circumstances
of ecology, as discussed later. Thus, the relative con-
servatism of the developmental mode within taxa of
familial and ordinal rank may reflect evolutionary con-
servatism of ecology rather than that of development.
scale. Among nonaltricial species, however, the dry
mass of the down, shown in Fig. 1.9 as a fraction of
the total dry mass of the chick, bears no particular re-
lationship to
IP
. Down mass varies among these spe-
cies from as little as 6.5% of the dry mass in the Adelie
penguin to 21% in the ducks and 26% in the alcids.
The functional maturity of the neonate has often
been related to the size of its brain. We calculated
residuals from the regression of log10(brain mass) and
log10(body mass) for the 46 species. Again, no rela-
tionship exists between residuals of the regression of
brain size on body mass and the dry matter content of
the neonate tissue, including the brain. The pronounced
differences in the relative sizes of the brain between
the groups included in this study presumably reflect
other aspects of development and ecology than the
actual functional maturity of the neonate.
From this analysis, we draw the following general,
albeit tentative, conclusions. (a) The functional maturi-
ties of five tissues that have different patterns of use
during development appear to vary in parallel, defin-
ing a single axis of variation in the functional maturity
of the neonate. (b) The lean dry fraction of the whole
neonate provides a useful scale of the developmental
grade. (c) Because lean dry fraction decreases with
increasing neonate mass, we have calculated an index
(IP)
that takes the mass of the neonate into account.
The index
IP
is the deviation of the observed lean dry
fraction from the allometric regression of the lean dry
fraction on the neonate mass. (d) On this functional
maturity scale, altricial species are distributed at low
values of
IP
and seem to be separated from nonaltricial
species that show a wide range of variation in func-
tional maturity in a higher range of
IP
. The results of
our analysis suggest variation along a unidimensional
and continuous spectrum of functional maturity that
contrasts with Nice’s (1962) categorical classification
1.6. 1.6.
1.6. 1.6.
1.6. A Mammalian PA Mammalian P
A Mammalian PA Mammalian P
A Mammalian Perer
erer
erspectispecti
spectispecti
spectivv
vv
vee
ee
e
As in birds, mammalian neonates exhibit a varying
degree of independence, ranging from extremely
altricial marsupials and monotremes to the relatively
independent young of ungulates. Compared to birds,
the mammalian embryo develops under fundamentally
different physiological and structural conditions that
place it in a different framework of selection and in-
ternal constraints. The most striking differences in re-
productive strategies of birds and mammals are as fol-
lows. (a) Birds are oviparous, whereas mammals are
viviparous (except for the oviparous monotremes). (b)
Nutrient supply to the mammalian embryo through the
placenta is continuous and almost unlimited as com-
pared to the energy-limited egg compartment in birds.
(c) The intrauterine development of the mammalian
embryo allows the mother a relative independence of
movement during almost all phases of its reproduc-
tive status, whereas birds incubate their eggs through
the whole embryonic period and are bound to the nest.
(d) Lactation allows the nourishment of neonates and
growing young mammals to be relatively independent
of the actual environmental conditions (e.g., immedi-
ate food abundance and weather conditions, which
have important effects on avian postnatal growth; see
chapter 16). (e) The costs of reproduction are almost
exclusively borne by the female in mammals, whereas

between altricial and precocial development; for ex-
ample, nonhuman primates are born with well-devel-
oped fur and open sensory organs but depend to a much
higher degree on parental care than do precocial
neonates. Different intermediate stages may be found
within orders. For example, within the rodents, mice
and rats (Muridae) produce highly altricial young,
whereas spiny mice (
Acomys inous
) and guinea pigs
(
Cavia
sp.) have highly precocial young (Fig. 1.10).
Bats (Chiroptra) show a similar diversity of neonates,
ranging from altricial young (Megachioptera), which
are born naked, to more precocial taxa (Phyllosoma-
toidea), which are born with open eyes and are cov-
ered with fur (Eisenberg 1981). Derrickson (1992)
developed a classification scheme for mammalian neo-
nates that employs developmental categories for neona-
tal independence in four areas: thermoregulation, sen-
sory organs, locomotion, and nutrition (Table 1.5).
Mammalian orders clearly exhibit greater flexibility
of developmental mode than do avian orders, with
Carnivora and Rodentia exhibiting the full range from
altricial to precocial.
23Patterns of Development: The Altricial-Precocial Spectrum
they are more equally partitioned among sexes in many
birds. The evolution of altricial and precocial neonates
under such different reproductive strategies makes an
interesting contrast between birds and mammals. Here,
we briefly outline similarities and differences in avian
and mammalian ontogenies to determine whether
altriciality and precocity refer to the same phenom-
enon in birds and mammals and to gain some insight
into the major selective conditions that drive the di-
versification of mammalian ontogenies. We review
current ideas and provide a perspective on mammals,
but we cannot give a comprehensive treatment in lim-
ited space.
1.6.1. 1.6.1.
1.6.1. 1.6.1.
1.6.1. TT
TT
The mammalian altrhe mammalian altr
he mammalian altrhe mammalian altr
he mammalian altricial-pricial-pr
icial-pricial-pr
icial-precocialecocial
ecocialecocial
ecocial
spectrumspectrum
spectrumspectrum
spectrum
The mammalian neonates show considerable differ-
ences in their developmental stage. For example, many
insectivores (Insectivora), all rabbits (Lagomorpha),
many rodents (Rodentia and Muridae), and most car-
nivores (Carnivora) give birth to small neonates that
have closed eyes and ears, and no hair, are generally
poorly developed, and are dependent on maternal care
for a long lactation period. Newborn marsupials and
monotremes are extremes, resembling early embryos,
even compared to other altricial mammals. Precocial
neonates are found among the ungulates (Cetacea,
Sirenia, Proboscidea, Hyracoidea, Perissodactyla, and
Artiodactyla), the Pinnipedia, and several rodent taxa
(Rodentia). Precocial mammals, especially ungulates,
may run swiftly and for long distances shortly after
birth, and some begin to feed on solid food within a
few days. The neonates of some taxa are intermediate
1.6.2. P1.6.2. P
1.6.2. P1.6.2. P
1.6.2. Poror
oror
ortmann’tmann’
tmann’tmann’
tmann’s vies vie
s vies vie
s vieww
ww
w
The general perception of the evolution of altricial and
precocial mammals has for a long period been domi-
nated by the ideas of Adolf Portmann and his student
Fabiola Müller. Although these ideas are difficult to
accept in the light of modern evolutionary biology, the
data and basic information provided with their publi-
cations are most valuable. Portmann’s concept encom-
passes four paradigms. (a) The evolution of avian onto-
genies proceeds from independent development toward
FF
FF
Figig
igig
ig. 1.10. . 1.10.
. 1.10. . 1.10.
. 1.10. Neonate of an altricial house mouse (
Mus musculus
, Muridae) and a precocial spiny mouse (
Acomys minous
,
Muridae) to demonstrate the diversity of neonates within Muridae, Rodentia (with kind permission of D. Starck).

24 Avian Growth and Development
Table 1.5. Developmental categories of neonates in mammalian orders (after Derrickson 1992). Black fields
indicate the major mode of development for that order; striped fields indicate that the specific mode of deve-
lopment occurs in few species only.
Order Altricial Intermediate Precocial
Insectivora
Macroscelididae
Chiroptera
Scandentia
Primates
Edentata
Pholidota
Lagomorpha
Rodentia
Cetacea
Carnivora
Pinnipedia
Tubulidentata
Proboscidea
Hyracoidea
Artiodactyla
lips (Müller 1968b, 1969, 1972a, 1972b, 1972c,
1972d). Within the eutherian mammals, insectivores,
rodents, and carnivores were thought to represent the
ancestral syndrome of altriciality as inherited from
marsupials, with a high number of young, a short ges-
tation period, and naked neonates whose eyes and ears
are closed and who cannot thermoregulate appropri-
ately. Portmann and Müller suggested that the diver-
sity of neonates in the “lower ranking orders of mam-
mals” — for example, within the rodents neonates may
be altricial (
Rattus norvegicus
, Muridae) or precocial
(
Cavia cobaya
, Caviidae) — represents evolutionary
trials toward the “next higher category.” Besides pro-
longation and abbreviation (shortening) of the gesta-
tion period, heterochrony in many organ systems (es-
pecially in the skeleton of the skull and legs) was rec-
ognized as an important mechanism of evolutionary
change of ontogenies (Schinz 1937; Müller 1972a,
1972b, 1972c, 1972d). Precocial eutherian mammals
comprise all marine mammals, primates, and ungu-
lates. The highest grade of ontogeny was suggested
for humans, who were thought to represent a second-
arily nidicolous species passing through the nidifugous
stage in utero (Portmann 1941, 1945, 1952, 1957,
1962). Although Portmann published extensively about
this topic, his ideas remained notably ambiguous con-
cerning retardation and acceleration of human embry-
onic development and how secondarily altricial young
could be precocial while embryos. An important gen-
eralization from Portmann’s studies is that the timing
increasing dependence of the embryo and neonate on
its parents. In contrast, mammalian ontogenies evolved
from altricial to precocial. (b) Ontogenies evolve in
categorical units (macroevolutionary changes) and may
be recognized by specific syndromes of altriciality or
precocity (Geigy and Portmann 1941), “morpholo-
gische Wertigkeit” in his terminology (Portmann
1938a, 1938b). (c) The evolution of ontogenies pro-
ceeds as the correlated evolution of organ systems and,
therefore, must be considered in relation to taxonomic
(phylogenetic) position rather than in the context of
the environment of the neonate. (d) Central to Port-
mann’s ideas is the “rule of precedence,” which as-
sumes that changes in the ontogenetic mode (e.g., the
conversion from nidicolous to nidifugous) must pre-
cede the evolution of specific structural characters of
precocity. For example, in mammals, the neonate must
become precocial before it can evolve a large neonate
brain size, thus resulting in an ordered evolution from
altricial to primitive precocial, which precedes the de-
rived precocial condition.
Briefly, the egg-laying monotremes, with very short
gestation periods, and small “embryonic” neonates
were considered the most ancestral condition. Their
ontogenetic mode was thought to represent a “miss-
ing link” between “reptiles” and mammals (Müller
1968a). Marsupialia were considered to be an inter-
mediate link to eutherian mammals because of their
poorly evolved parental (maternal) care for the young,
and embryonic and postnatal closure of eyes, ears, and

25Patterns of Development: The Altricial-Precocial Spectrum
of birth in mammals is much more flexible than the
timing of hatching in birds. Also, heterochrony was
recognized in the development of specific organ sys-
tems (e.g., the forelimbs, mouth, intestinal tract, and
lungs of marsupials), resulting in the considerable di-
versity of mammalian neonates.
Reproductive strategies in monotremes, marsupi-
als, and eutherian mammals are not simply a sequence
of evolutionary grades but rather represent independ-
ently derived specializations in each group. For exam-
ple, this can be seen on the structural level by the de-
rived structure of mammary glands and in the physiol-
ogy of lactation. Most marsupials develop a choriovi-
telline placenta (yolk-sac placenta), whereas the euthe-
rian mammals rely on a chorioallantoic placenta (allan-
tois placenta); only the bandicoots (
Perameles
spp.)
have both (Renfree 1983; Tyndale-Biscoe and Renfree
1987). A phylogenetic analysis of amniotic fetal mem-
branes suggests that the reduction of an extensive
chorioallantoic placenta should be considered a de-
rived character (Luckett 1977). Further specializations
of the neonate marsupial, for example, the highly func-
tional tongue musculature and the functionality of the
mesonephros (embryonic kidneys), are described by
Hughes and Hall (1988). It has been pointed out by
Renfree (1983) that mammalian reproduction evolved
along two alternative avenues, one favoring the lacta-
tion strategy, as in marsupials, the other favoring ges-
tation, as in eutherian mammals. For marsupials, ex-
tended lactation apparently was the more successful
reproductive strategy, allowing for very small young,
which had unlimited potential for growth when condi-
tions were good but could be easily jettisoned under
adverse conditions.
ward relationship between mode of development and
r
or
K
strategy. Altricial development is found among
insectivores and rodents, usually thought of as
r-
se-
lected taxa, as well as edentates (anteaters and sloths),
which represent typically
K-
selected taxa. Monotremes
have extremely altricial neonates but a low reproduc-
tive rate, intensive parental care, and slow postnatal
development; platypus (
Ornithorhynchus anatinus
)
and echidna (
Tachyglossus aculeatus
) would be char-
acterized as typical
K-
strategists. Precocial species,
however, are found among large ungulates and aquatic
mammals (cetaceans and manatees), which are seem-
ingly
K-
selected, as well as rodents (
Cavia
) and
hyracoids (
Hyrax
), which typically are
r-
selected
(Fischer 1992). Gould (1977) considers heterochrony
to be a driving force in the evolutionary diversifica-
tion of ontogenetic modes in mammals and extended
this idea to hypothesize a paedomorphic origin of hu-
mans from other primate genera (for reviews, see Bolk
1926; D.Starck 1962, 1974, 1975; Gould 1977; Shea
1988).
20 Progenesis: paedomorphosis (retention of formerly juvenile
characters by adult descendants) produced by precocious se-
xual maturation of an organism still in a morphologically ju-
venile stage (Gould 1977).
21 Hypermorphosis: the phyletic extension of ontogeny beyond
its ancestral termination (usually to a larger body size).
1.6.4. Lif1.6.4. Lif
1.6.4. Lif1.6.4. Lif
1.6.4. Life histore histor
e histore histor
e history ay a
y ay a
y apprppr
pprppr
pproacoac
oacoac
oachh
hh
h
Eisenberg (1981) placed mammalian ontogenies in the
context of life history evolution. He described two
major trends in the diversification of ontogenies. On
the one hand, large adult body size favors the produc-
tion of large, precocious young, which develop during
a long gestation period and thus, to some degree, de-
pend on the reliable availability of food for their moth-
ers. Large neonates are thought to correlate with a long
life-span, an extended period of reproduction, and re-
duced litter size. On the other hand, Eisenberg sug-
gested that altricial mammals were selected for the
ability to “recycle” their young (that is, the mother may
resorb the embro at any stage of its development), thus
regaining invested energy at any point of the repro-
ductive cycle, when adverse environmental conditions
would prohibit the successful rearing of young. This
conceptual framework has been supported anecdotally
by observational evidence but certainly should be ex-
amined more closely, particularily to determine
whether development is associated closely enough with
ecology for an explanation of the within-order diver-
sity of neonates (e.g., Rodentia and Carnivora). Re-
cent studies of neonate brain size, mode of develop-
ment, and life history traits (Martin 1981, 1984;
Bennett and Harvey 1985; Grand 1992) have supported
Portmann’s view of a strong relationship between pre-
cocial development and large neonatal brain size. How-
ever, these studies rely on a basically dichotomous
perception of development and cannot explain the ob-
vious variation within taxonomic groups.
Derrickson (1992) used four categorical traits (ther-
moregulatory, sensory, locomotory, and nutritional) to
characterize mammalian neonates (Table 1.5). Inde-
pendence in all four traits was assigned to precocial
1.6.3. Heter1.6.3. Heter
1.6.3. Heter1.6.3. Heter
1.6.3. Heterococ
ococ
ochrhr
hrhr
hronon
onon
ony and mammaliany and mammalian
y and mammaliany and mammalian
y and mammalian
dede
dede
devv
vv
velopmentelopment
elopmentelopment
elopment
Gould (1977, p. 349; 1988) presents a general hypo-
thesis of heterochrony in mammalian ontogeny, mostly
based on Portmann’s work and relating it to patterns
of selection. He attempts to understand macroevo-
lutionary changes by relating progenesis20 and altricial
development (early maturation) to
r
-selection, and pro-
longation of development (hypermorphosis,21 with
extended periods of differentiation) and precocity to
K-
selection. However, even if we would adopt the view
relating diversification of ontogenies to patterns of
selection, it is difficult to recognize any straightfor-

0123
Neonate mass
-0.2
0.0
0.2
Neonate mass
0123
Gestation period
-0.2
0.0
0.2
Incubation period
ASASPP
ASASPP
Mammals Birds
development, and dependence in all four to altricial,
with intermediate stages exhibited by a variety of taxa.
Neonates were then compared in nine life-history traits.
The results of her analysis show that (a) the length of
the gestation period is extended in precocial primates
but shortened in precocial rodents; (b) the neonate mass
varies according to developmental category, (c) the lit-
ter size and growth rate vary dichotomously along the
altricial-precocial spectrum; (d) litter mass and age of
first parturition show no significant variation among
developmental categories. Derrickson’s analysis shows
clearly that mammalian neonatal patterns have not
evolved along a single continuous axis of diversifica-
tion and that altricial and precocial development prob-
ably arose independently in response to more than one
kind of selection pressure. According to Derrickson’s
analysis, the concept of an altricial-precocial spectrum
in mammals differs strikingly from that in birds. In
mammals, the developmental mode is highly corre-
lated with the neonate size and gestation period, sug-
gesting that the developmental advancement of preco-
cial species reflects a prolongation of the embryonic
developmental period but perhaps not an increase in
maturation with respect to growth, as is apparent in
birds (Fig. 1.11).
26 Avian Growth and Development
FF
FF
Figig
igig
ig. 1.11. . 1.11.
. 1.11. . 1.11.
. 1.11. Comparison of the (a) mammalian and (b) avian altricial-precocial spectrum. The upper penels show averages and
standard deviation of residuals from an allometry of the neonate mass on body mass for four developmental categories; the
lower panels show residuals from an allometry of gestation period (incubation period) on adult body mass. The developmental
categories for mammals follow Derrickson (1992); 0, altricial; 1 and 2 intermediate forms; 3, precocial. For birds; A, altricial;
SA, semialtricial; SP, semiprecocial; P, precocial.
1.7. Conclusions1.7. Conclusions
1.7. Conclusions1.7. Conclusions
1.7. Conclusions
The analysis of lean dry fraction suggests that the de-
velopmental mode in birds varies continuously along
a single dimension. If this reflects evolution correctly,
one may conclude that evolutionary diversification of
ontogenies has followed gradual rather than categori-
cal changes. The only clear contrast in the index of
lean dry fraction
IP
appears between altricial birds and
all other birds, including semialtricials. At present, we
cannot resolve whether this is a true gap or whether
additional data might fill the space between altricials

27Patterns of Development: The Altricial-Precocial Spectrum
ferent organ systems and its variation in only a single
dimension suggests that the overall similarity of
altricial or precocial chicks of different taxa represents
parallel evolution rather then similarity based on com-
mon ancestry.
When it is difficult to reconstruct the ancestral char-
acter state of developmental modes through phyloge-
netic analyses, we might proceed by investigating eco-
logical characteristics of extinct ancestral avian taxa
that are predictive of developmental mode. For exam-
ple, precocial chicks always have to search for food
on the ground, have a wide spectrum of food items,
and gather easily accessible prey. Altricial young how-
ever, may relay on the prey capture skills of their par-
ents and thus may be fed a food that is inaccessible for
precocials. We return to this question in chapter 16.
and other groups. Regardless, values of
IP
in altricial
birds appear only to extend the range of variation ex-
hibited by all other birds along a single dimension.
Thus, we recognize a continuous gradient of functional
maturity comprising all developmental modes, in
which altricial birds exhibit values of
IP
beyond the
ranges of all other developmental modes. It is impor-
tant to note that except for altricial birds, traditional
categories of development (e.g., Nice 1962) cannot be
distinguished by unique ranges of
IP
values. For ex-
ample, precocial and semiprecocial birds (in Nice’s
category) occupy a wide range of
IP
values, overlap-
ping at the lower end of the range with semialtricial
birds. Thus, realizing that continuous and overlapping
variation of functional maturity underlies most catego-
ries of development, we might be wiser to recognize
only altricial development as a quantitatively distinct
category. Attention should focus on understanding the
basis for variation in functional maturity among all
other birds as well as the uniqueness of altricial devel-
opment.
The analysis leaves us with a set of questions that
are difficult to answer. What actually causes evolu-
tionary change in lean dry fraction or
IP
? Is the sched-
ule of development changed so that
IP
represents dis-
tance along the developmental progress of maturation?
Several lines of evidence discussed in the next chap-
ter (see also J.M. Starck 1989, 1993) suggest that this
is not the case and that the time patterns of develop-
ment are rather unchanged in birds.
Another puzzling question concerns why the ap-
parent functional levels of all tissues except liver
change together. Why is variation in avian develop-
ment organized along a single dimension? Our data
support earlier studies by O’Connor (1977, 1978a,
1978b) which suggest that developmental processes
are tied together in such a way that changes in any one
tissue must be accompanied by changes in all others.
That is, development is a phenomenon of the whole
organism rather than independent phenomena of indi-
vidual tissues, in spite of the fact that the onset of func-
tion in different tissues seems to vary independently
of their developmental schedules.
Finally, what is the meaning of the relation between
neonate mass and lean dry fraction? Why should larger
species tend to have lower function and capcity, par-
ticularly as they seem to show greater independence
as neonates?
Phylogenetic analyses of mode of the development
could not clearly resolve whether altricial or precocial
development was the ancestral trait in birds. Multiple
independent origins of altriciality and precocity are
highly probable from the phylogenetic comparisons.
The probability of an independent evolutionary origin
of altriciality in dinosaurs indicates that the mode of
development might have changed frequently during
evolution. The high integration of development of dif-
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