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Behavioral Ecology Vol. 11 No. 4: 367-377
© 2000 International Society for Behavioral Ecology
Prolonged offspring dependence and cooperative breeding in birds
Department of Organismic Biology, Ecology and Evolution, University of California, Los Angeles, CA 90095-1606, USA
Address correspondence to T. Langen at the Department of Biology, Clarkson University, PO Box 5805, Potsdam, NY 13699-5805, USA. E-mail : tlangen{at}clarkson.edu .
Received 7 June 1999; revised 11 October 1999; accepted 25 October 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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It has been suggested that the evolution of cooperative breeding in birds is associated with unusually long periods of offspring dependence ; this appears paradoxical because cooperative breeders often produce more broods than their noncooperatively breeding relatives. I compared the duration of parental care between cooperatively and noncooperatively breeding species using phylogenetically independent contrasts and matched pairs. The incubation and nestling periods did not differ between the two parental care systems, but the duration of postfledging offspring care was significantly longer in species that regularly breed cooperatively. This relationship remained when other factors that are thought to affect the duration of fledgling care (breeding habitat, body size, latitude of breeding, diet) were controlled statistically. Cooperative breeders appear to provide more prolonged postfledging care because additional care providers reduce the costs of parenting, offspring have less incentive to become independent, and a division of labor can develop during reproduction—helpers continue to feed fledglings while breeders initiate the next nesting attempt.
Key words: avian reproduction, cooperative breeding, life-history trade-offs, parental care..
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Parents may provide several forms of care for their off-spring : warmth, access to resources, protection from predators, and food (Clutton-Brock, 1991
). In
cooperatively breeding birds, other individuals contribute to the care of the
young in addition to the genetic parents. For some of these species,
cooperative breeding results in a greater number of offspring or more viable
offspring in each brood because of a decreased risk of starvation or predation
(reviewed in Brown, 1987 ;
Cockburn, 1998 ;
Emlen, 1991). It has been
suggested that offspring of cooperatively breeding birds receive more
prolonged care than noncooperative breeders
(Heinsohn, 1991 ;
McGowan and Woolfenden, 1990),
but there has been little comparative evidence published to support this
conjecture.
A few life-history traits have been shown to be associated with cooperative
breeding, including higher adult survivorship, smaller clutch sizes, and more
broods per breeding season than noncooperative breeders
(Arnold and Owens, 1998 ;
Brown, 1987 ;
Poiani and Jermiin, 1994). In
most species of birds, parentai care of a brood is terminated soon after the
production of the next brood begins (e.g.,
Verhulst and Hut, 1996 ;
Weatherhead and McRae, 1990 ;
With and Balda, 1990 ;
Zaias and Breitwisch, 1989).
By prolonging brood care, parents may increase the survivorship of offspring,
at the costs of deferred production of the next brood or a reduction in their
own survivorship (Davies, 1976
; Verhulst et al., 1997 ;
Weathers and Sullivan, 1989).
It seems paradoxical that cooperatively breeding birds can both produce more
broods and provide more extensive care than noncooperative breeders.
Unfortunately, the main causes of variation in the duration of offspring
care remain uncertain. For example, there is continuing controversy over which
factors have the greatest effect on the duration of incubation and nestling
care : diet, predation, or sibling competition
(Lack, 1968 ;
Martin, 1995 ;
Ricklefs, 1993). Even less is
known about the duration of care once offspring have left the nest
(Nice, 1943 ;
Skutch, 1976), yet for many
species the longest period of offspring care and the peak rate of offspring
provisioning occurs after fledging (e.g.,
Langen and Vehrencamp, 1999 ;
McGowan and Woolfenden, 1990 ;
With and Balda, 1990). The
duration of postfledging offspring care may be influenced by (1) body size, as
are the length of incubation, postantal metabolic rate, and many other
life-history traits (Daan and Tinbergen,
1997 ; Lack, 1968
; Weathers and Siegal, 1995)
; (2) latitude of breeding, with tropical and southern hemisphere temperate
species providing more extensive care than northern hemisphere temperate
species (Ricklefs, 1969 ;
Rowley and Russell, 1991) ;
(3) diet, with birds that exploit food that is difficult to locate, capture,
or process having prolonged offspring care
(Ashmole and Tovar, 1968 ;
Fogden, 1972 ;
Heinsohn, 1991 ;
Higuchi and Momose, 1981) ;
and (4) the conflicting interests of offspring and parents
(Mock and Forbes, 1992 ;
Trivers, 1974).
Many resemblances among cooperatively breeding species can be attributed to
shared ancestry (Cockburn,
1996 ; Edwards and Naeem,
1993 ; Ligon,
1993). I compared the duration of parental care between
cooperative and noncooperative breeders after controlling for statistical
non-independence due to phylogenetic relatedness and for ecological variables
that may also affect this duration. Here I discuss why these parental care
systems might differ in the duration of parental care and speculate on the
evolutionary consequences of such a difference.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Estimating the duration of offspring dependence
Measuring the duration of incubation and nestling care is straightforward, but there is no standard way to estimate the duration of parental care once offspring have left the nest. In this study, I compared the lengths of time that offspring are fed by parents or others after fledging, called the duration of postfledging nutritional dependence. This duration includes both the period that offspring are completely dependent on parents for food and the additional period in which offspring can potentially self-feed but benefit from parental provisioning during shortfalls that occur while young acquire foraging skills (Langen, 1996
; Sullivan, 1988). The
duration of postfledging nutritional dependence should reflect the duration of
offspring care but is not necessarily related to the peak magnitude or total
magnitude of parental effort (e.g., the peak rate of provisioning or the
cumulative amount of food provided to offspring).
The age at which offspring become completely self-feeding is undoubtedly
less accurately estimated than dates of hatching or fledging
(Skutch, 1976). This is due
in part to the inherent difficulties associated with observing young birds
after they leave the nest. Moreover, there can be considerable intraspecfic
variation in the duration of nutritional dependence depending on whether
parents have an opportunity to renest (last broods are provisioned longer than
others ; Nice, 1943 ;
Skutch, 1976), the abundance
of food (offspring have longer periods of dependence when food is scarce ;
Byle, 1990 ;
Seki and Takano, 1998 ;
Yoerg, 1998), and brood size
(individuals from large broods become independent earlier ;
Heinshon, 1991). Imprecise
estimates of the mean duration of nutritional dependence due to these factors
may obscure correlations with other life-history variables but are unlikely to
create spurious associations.
However, there are at least three reasons that there might be a directional
measurement bias in estimates of the duration of postfledging nutritional
dependence associated with a parental care system. First, some observers may
confound food exchanges that function as a form of social bonding with
parental care. Such allofeeding occurs in cooperatively breeding Arabian
babblers Turdoides squamiceps, Florida scrub-jays Aphelocoma
coerulescens, and other species
(McGowan and Woolfenden, 1990
; Zahavi, 1990). Second,
scrounging or stealing food by juveniles, which occurs commonly in many
species of birds (Wunderle,
1991), may sometimes be classified erroneously as parental
provisioning within groups of cooperative breeders. Finally, family groups of
cooperative breeders may have greater territorial fidelity than others and
hence are easier to locate and monitor than noncooperative breeders that
provide equally prolonged care.
I evaluated these possibilities by comparing the results from the entire data set (see below) with those derived from a subset of studies in which the duration of nutritional dependence appeared to have been estimated with the most precision. This subset was composed of those studies in which parental food provisioning behavior was repeatedly quantified at regular, short intervals until offspring were entirely self-feeding, for more than one brood. Bias would be indicated if there were a trend in the residuals toward positive or negative deviations from zero. Systematic negative residuals among the cooperative breeders suggest that other, less careful studies tend to overestimate the duration of nutritional dependence in this group, whereas positive residuals for the noncooperative breeders indicate that most other studies underestimate the duration for this group.
Sources of comparative data
Members of the large monophyletic avian order Passeriformes are
ecologically diverse, but the young of all species are altricial and require
feeding by adults. Searching three encyclopedic collections of avian life
histories (Brown et al.,
1982-1997 ; Cramp and Perrins,
1977-1994 ; Poole et al.,
1990-1997), all issues between 1970 and 1998 of several major
ornithological journals (Auk, Condor, Emu, Ibis, Notornis, Ornis
Scandinavica, Ostrich, Wilson Bulletin) and other sources, I found 261
species of Passerine birds for which an estimate of the duration of
nutritional dependence in the wild has been made. I also noted the duration of
nutritional dependence among species in nonpasserine clades that include
cooperative breeders and that feed their young, including semi-precocial and
altricial species. I included all sources that contained an estimate of the
duration of nutritional dependence, regardless of whether the authors provided
explicit details on how such estimates were made (data available by request).
I recorded the mean duration of nutritional dependence (in days) for each
species, or the midpoint of the range of ages if no mean was reported.
For each species in the data set, I also recorded the mean (or mid)
incubation period and age at fledging (in days), mean adult female body mass
(in grams, unsexed adult mass used if female mass unknown), and annual
survivorship if measured. For asynchronously hatching species, the mean
incubation period for the total brood was recorded (i.e., from the initiation
of sustained incubation until half the clutch had hatched). The duration of
care of the first brood of a breeding season was used when specified. Body
masses were recorded primarily from Dunning
(1993) or from the cited
source.
I also noted the latitude of breeding, breeding habitat, and adult diet of each species. Breeding latitude was categorized as (1) northern hemisphere temperate, (2) southern hemisphere temperate, or (3) tropical. If a species breeds at more than one of these latitudes, I used the latitude at which the duration of nutritional dependence was estimated. Habitat was categorized as (1) forest (closed canopy of trees), (2) mixed (noncontinuous tree cover including savannah, gardens, and agricultural areas), or (3) open (desert, grassland, and marsh). Adult diet was categorized by the proportion of animal food (arthropods, vertebrates, etc.) and vegetable food (fruit, seeds, and nectar) as : (1) primarily animal, (2) mostly animal, some vegetable, (3) mostly vegetable, some animal, or (4) primarily vegetable. Migratory status was also recorded, but because virtually all migratory species were northern hemisphere temperate in my data set and none was cooperatively breeding, this factor was not included in the analyses.
Finally, each species was categorized into three groups according to the
size of the breeding unit : frequently cooperatively breeding species (rank =
3) are those in which the mean number of birds that regularly feed offspring
averages 2.5 or more per breeding unit in at least one studied population
(these include both species with nonbreeding helpers and species with more
than 2 genetic parents per brood) ; noncooperatively breeding species (rank =
1) are those with a mean of 
2.0 adults that feed offspring in all studied
populations ; and occasionally cooperatively breeding species (rank = 2) are
those species for which the mean is intermediate (2.1-2.4).
Treatment of comparative data
I used the computer application Comparative Analysis by Independent
Contrasts (CAIC) 2.0 (Purvis and Rambaut,
1995) to calculate standardized phylogenetically independent
contrasts for statistical analysis (for justifications and underlying
evolutionary and statistical assumptions, see
Felsenstein, 1985 ;
Martins and Hansen, 1996 ;
Pagel, 1992). The duration
measures and body mass were natural-log transformed, and survivorship was
arcsine transformed before calculating the contrasts. Branch topology of the
phylogeny was based on Sibley and Ahlquist
(1990) at deeper nodes and
other recent phylogenies if available at terminal nodes (phylogenies :
Badyaev, 1997 ;
Bledsoe, 1988 ;
Espinosa de los Monteros and Cracraft,
1997 ; Freeman and Zink,
1995 ; Johnson et al.,
1988 Lanyon, 1994
; Leisler et al., 1997 ;
Patten and Fugate, 1998 ;
Peterson and Burt, 1992 ;
Price et al., 1997 ;
Rowley and Russell, 1997 ;
Sheldon and Winkler, 1993 ;
Sheldon et al., 1992 ;
Zink and Blackwell, 1996).
Species that did not appear on any phylogeny were placed adjacent to relatives
that did, relatedness inferred from the standard taxonomy in Sibley and Monroe
(1990). If no other
information was available, I assumed that species in the same genus were more
closely related than species in sister genera. Branch lengths were estimated
using Sibley and Ahlquist
(1990) data at 1.0 delta
T50H units or greater and equal branch lengths below (= 1.0 delta
T50H units) because branch lengths from other phylogenies were not
comparable. I used Garland et al.'s
(1992) method to appropriately
scale the branch lengths ; those used in the reported analyses were
natural-log transformed. However, using untransformed branch lengths or
setting all branch lengths equal did not qualitatively change the results.
For bivariate comparisons of truly continuous variables, I calculated
standardized phylogenetically independent contrasts using the CAIC 2.0 option
CRUNCH [this option calculates contrasts using the method of Felsenstein
(1985) as modified by Pagel
(1992) for non-bifurcating
nodes on a phylogeny]. The option BRUNCH was used for comparisons that
included one ranked categorical variable (BRUNCH uses parsimony to estimate
the evolutionary pattern of the categorical variable, then calculates
contrasts of a continuous variable at nodes where there is a transition from
one categorical state to another). In the BRUNCH analyses, the association
between the dependent variable and the independent variable was tested via
sign tests, since the contrasts of the ranked variable were scaled relative to
the lowest such that the null expectation (no difference between ranks)
equaled zero. To produce a general linear model using multiple ranked and
continuous variables, I used the CRUNCH option to calculate contrasts [for a
justification of this approach, see Grafen
(1989) and a brief discussion
in Purvis and Rambaut
(1995)]. The distribution of
the residuals was inspected to verify the assumption of normality
(Grafen, 1989). Regressions
were fit through the origin (Garland et
al., 1992).
Depending on how traits have evolved and the magnitude of estimate errors,
there is evidence that analyses based on raw species data provide different
information, and are sometimes more appropriate, than phylogenetically
independent contrasts (Price,
1997 ; Ricklefts and Stark,
1996). Therefore, throughout this paper I report duplicate
statistical analyses using both the independent contrasts and the raw species
data. In each case, durations were natural-log transformed before
analysis.
Finally, I also used a matched-pairs comparative method
(Felsenstein, 1985 ;
Møller and Birkhead,
1992), limiting comparisons of offspring care duration to closely
related taxa that differ primarily in the parental care system. The chief
weakness of using matched pairs over independent contrasts or other methods is
that many potential comparisons are excluded and hence statistical power is
lowered. This results in conservative statistical tests, but fewer assumptions
are made about how the traits have evolved than when using other comparative
methods (Harvey and Nee, 1997
; Ridley and Grafen,
1996).
I compared frequently cooperatively breeding taxa with sister taxa of
noncooperative breeders, using data from some of the passerine species
included in the independent contrasts analyses and additional nonpasserine
taxa. Occasional cooperative breeders were not used in the matched-pairs
analyses but are mentioned in the results if they lie within a clade used in
the comparisons. To identify the appropriate pairings, I primarily relied on
the phylogenies used in the independent contrasts analyses (above), but
alternative pairings were also used when other sources disagreed with these.
The most distantly related pairings used in the analyses were at the subfamily
level [maximum distance from Sibley and Ahlquist
(1990) data = 7.5 delta
T50H units, mean ± SE = 2.9 ± 0.56]. No taxon was
included in more than one matched pair.
When I had data from multiple species within a clade, I used the mean species value in the comparisons. In a few instances, more than one species with each parental care system shared a node on the phylogeny ; for these the mean value of all cooperative breeders was compared to the mean of the noncooperative breeders. Substituting medians for means in the analyses did not alter the results. Sign tests were used as statistical tests of whether general patterns exist in the direction of differences between matched pairs, uninfluenced by the magnitude of the differences.
For a subset of matched pairs, published phylogenetic reconstructions of
the evolution of parental care systems exist (such reconstructions assume
parsimony and use many more species than are included in the matched pairs ;
e.g., Edwards and Naeem, 1993
; Peterson and Burt, 1992).
These studies allowed me to infer whether cooperative breeding was ancestral
or derived within the matched pair. For some other matched pairs, I could
infer that the ancestral state of the parental care system was noncooperative
breeding because, with the exception of the cooperative breeding species of
the matched pair, other species within the genus and closely related genera
are noncooperative breeders. I used these reconstructions to ask whether
directional changes in the duration of care were equally frequent when the
parental care system changed in either direction.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Independent contrasts and raw species data
Among the 261 species of passerine birds in my data set, the average duration of offspring care after leaving the nest (as measured by the duration of food provisioning) is nearly equal in duration to the total period of care within the nest (mean ± SE days : incubation period = 14.1 ± 0.15, nestling period = 15.7 ± 0.36, fledgling period = 27.3 ± 1.50). The period of care after fledging is much more variable among species than the incubation and nestling periods (coefficient of variation ± SE : incubation = 17.2 ± 0.79%, nestling = 37.2 ± 1.85%, fledgling = 89.1 ± 6.27%).
Frequently cooperatively-breeding passerine birds do not differ from noncooperative breeders in incubation duration per brood judging from the independent contrasts (11 of 18 contrasts > 0, sign test p =.5), although the raw species data suggest that cooperative breeders incubate longer (t240 = 3.2, p =.002 ; frequent cooperative, mean ± SE = 15.3 ± 0.50 days, n = 33, noncooperative breeders = 13.9 ± 0.16, n = 209). Time in the nest after hatching does not differ between the two parental care categories in passerine birds (9 of 19 contrasts > 0, sign test p = 1.0 ; raw species t245 = 1.6, p =.12 ; frequent cooperative breeders = 17.0 ± 1.00 days, n = 34, noncooperative breeders = 15.4 ± 0.40, n = 213). However, the contrasts for the duration of fledgling feeding are significantly higher for frequent cooperative breeders than for occasional cooperative breeders and noncooperative breeders (frequent cooperative breeders : 20 of 20 contrasts > 0, sign test p <.0001 ; occasional cooperative breeders : 5 of 9 contrasts > 0, sign test p = 1.0). This supports the pattern indicated by the raw species data (Figure 1 ; F2, 258 = 30.6, p <.0001).
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Using either contrasts or raw species data, the parental care system is a significant predictor of the duration of fledgling feeding in a multiple regression that also includes diet, habitat, latitude, and mass as predictors (Table 1 ; contrasts full regression model, F5, 185 = 18.2, p <.0001, r2 =.31 ; raw species full regression model, F5, 255 = 44.6, p <.0001, r2 =.46). This regression also indicates that offspring dependence is longer when the diet consists of animal food, the habitat occupied is woodland, breeding latitude is tropical, and body size is large (Table 1). Incubation or nestling care duration is not significantly associated with the breeding system when these other factors are included in a multiple regression model.
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To test whether there is a directional bias in the estimates of the age of nutritional independence associated with the parental care system, I calculated the residuals of the multiple regression of raw species data presented in Table 1. I then inspected the standardized residuals of the subset of studies that estimated the age of nutritional independence with greatest precision (Table 2 ; data include 4% of the noncooperative breeders and 12% of the frequent cooperative breeders). Neither the standardized residuals for the frequent cooperative breeders nor those of the noncooperative breeders differ significantly from zero (frequent cooperative breeders : t3 = 0.9, p =.5 ; noncooperative breeders : t7 = 0.1, p =.9).
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Finally, among the subset of species for which there are data on annual survivorship, the duration of fledgling feeding is significantly correlated with adult survivorship (contrast, r =.30, p =.007, n = 80 ; raw species, r =.38, p =.0002, n = 92). This correlation remains if the shared association with body mass is partialed out. The parental care system remains a significant predictor of the duration of fledgling dependence when survivorship is included in a regression model (parental care : contrast F1, 76 = 2.0, p =.04, standardized regression coefficient =.202 ; survivorship : contrast F1, 76 = 1.8, p =.08, coefficient =.198).
Matched pairs
The matched pairs of passerines (16 pairings) and nonpasserines (7
pairings) are described in the Appendix. Duration of incubation does not
differ significantly between the matched pairs (frequent cooperative breeders
longer in 13 of 20 non-tied comparisons, sign test, p =.3), nor does
the length of time between hatching and fledging (frequent cooperative
breeders longer in 8 of 16 non-tied comparisons, sign test, p = 1.0).
However, cooperatively breeding species do feed offspring significantly longer
after fledging (frequent cooperative breeders longer in 21 of 23 comparisons,
sign test, p <.0001). On average, they feed offspring twice as
long as their noncooperative relatives [median ratio
(cooperative/noncooperative) = 2.05]. As a consequence, the postfledging
period accounts for a relatively higher proportion of the total duration of
offspring investment between the initiation of incubation and the age of
nutritional independence [frequent cooperative breeders higher in 21 of 22
non-tied comparisons, sign test, p <.0001 ; median ratio (duration
of postfledging feeding/duration of nest care) : frequent cooperative breeders
= 1.27, noncooperative breeders = 0.73].
Using alternative phylogenies to create matched pairs does not
qualitatively change the results, nor does limiting pairings to very closely
related taxa (subtribe and below) based on the Sibley and Ahlquist
(1990) DNA-DNA hybridization
criterion, nor does restricting matched pairs to those consisting of species
in the same genus. Limiting comparisons to species-pairs that are similar in
body size, that breed in the same habitat or at the same latitude, or that
share diets does not qualitatively change the results either.
Noncooperative breeding is likely to have been the ancestral state in eight of the matched pairs, and cooperative breeding is likely to have been the ancestral state in six pairs (ancestral state of other pairs uncertain ; see Appendix). Among these pairs, it is as likely for the evolution of cooperative breeding to be associated with an increase in duration of fledgling care (seven of eight pairs) as it is for the loss of cooperative breeding to be associated with a reduction (five of six pairs ; Fisher's Exact test, p = 1.0).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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General conclusions
The results can be summarized by four main points. (1) The total duration of parental care at the nest (incubation and nestling periods) does not differ between cooperatively and noncooperatively breeding taxa. (2) Cooperatively breeding taxa do feed fledged offspring significantly longer than noncooperative breeders, and this association is not merely the result of other factors such as diet or latitude of breeding that covary with both the parental care system and the duration of postfledging care. (3) Changes in the parental care system in either direction (cooperative to noncooperative or the reverse) are both associated with directional changes in the length of postfledging offspring care. (4) Adult survivorship and the duration of fledgling feeding are positively associated. Cooperative breeders generally have higher adult survivorship than other birds (Arnold and Owens, 1998
;
Brown, 1987). However, the
duration of postfledging offspring dependence remains directly associated with
the parental care system when adult survivorship is statistically
controlled.
The first point may appear surprising ; one might expect that the duration
of care at the nest would be shorter in cooperative breeders because a larger
workforce could permit more sustained incubation and a higher rate of nestling
provisioning, resulting in a faster rate of offspring growth and therefore
earlier fledging to escape the risky nest environment. This would be
advantageous because the rate of prediation does not differ between
cooperatively and noncooperatively breeding species
(Poiani and Pagel, 1997).
Nevertheless, provisioning rate does not increase substantially with
additional members in the workforce in many cooperatively breeding species
(Brown, 1987 ;
Crick, 1992 ;
Hatchwell, 1999).
The second and third points confirm a modified form of the generalization
that cooperatively breeding birds provide more extensive care for their
offspring. There is a strong association between the length of postfledging
feeding and the parental care system such that transitions in either direction
are almost invariably associated with a predictable change in the duration of
care. It is not possible to conclude definitively with these correlative data
whether cooperative breeding causes a lengthening of parental care or whether
taxa that provide extensive care are predisposed to evolve cooperative
breeding, but the former is more probable. When closely related species differ
in both the parental care system and the duration of parental care, there are
no obvious differences in their reproductive biology or life history that
explain why the offspring of the cooperatively breeding species intrinsically
require more prolonged feeding by adults. Other ecological and social factors
seem to provide better general explanations for the evolution of cooperative
breeding in birds than inherently long offspring dependence (reviewed in
Brown, 1987 ;
Emlen, 1991 ;
Koenig et al., 1992). However,
the benefits to breeders and offspring from helper contributions that result
in extended brood care may help explain the maintenance of helping behavior
(see below).
It could be informative to examine how the duration of offspring dependence
varies within a species depending on the number of care providers. I am aware
of only two such studies : in white-winged choughs (Corcorax
melanorhamphos) the average duration of postfledging nutritional
dependence increases with the number of helpers
(Heinsohn, 1991), but in
dunnocks (Prunella modularis), offspring in breeding units of three
adults are not nutritionally dependent significantly longer than those with
two adults (Byle, 1990).
Potential causes and evolutionary consequences of prolonged
offspring care
In noncooperatively breeding birds, there is typically little overlap
between care of one brood and the production of the next, although a male may
continue to feed fledglings for a brief period on his own while his mate
begins to renest (e.g., Verhulst and Hut,
1996 ; Weatherhead and McRae,
1990 ; With and Balda,
1990 ; Zaias and Breitwisch,
1989). The duration of fledgling care is thought to be a
compromise between the length of time that most improves the viability of the
offspring and the length of time that allows the most nesting attempts during
the breeding season or least affects the parents' survival. Parental
provisioning is terminated when the costs to each parent are no longer
compensated by sufficient improvement in the condition of the offspring
(Davies, 1976,
1978 ;
Verhulst et al., 1997 ;
Weathers and Sullivan, 1989).
Offspring often appear to conflict with parents over the termination of
offspring care and may force parents to provide care for a somewhat longer
period than is optimal for them, but there is currently little empirical
evidence to support this conjecture (Mock
and Forbes, 1992 ; Trivers,
1974).
In cooperatively breeding species, helpers lighten the load on the breeders
by sharing in offspring care. Brood size is often unaffected by helper
contributions (Brown, 1987 ;
Crick, 1992 ;
Hatchwell, 1999). Instead, the
reduced burden on breeders results in higher survivorship for them or more
rapid renesting (Brown, 1987 ;
Poiani and Jermiin, 1994). In
some species, rapid renesting is facilitated by a division of labor within
cooperatively breeding groups : helpers continue to feed fledged young while
breeders begin the next nesting attempt
(Brown and Brown, 1981 ;
Carlisle and Zahavi, 1986 ;
Langen and Vehrencamp, 1999 ;
Rowley and Russell, 1990).
For example, in white-throated magpie-jays (Calocitta formosa),
renesting can coincide with the peak period of offspring provisioning, which
occurs soon after the first brood has fledged. Helpers do virtually all
subsequent provisioning of the first brood while a breeding pair begins
production of the second. If the second nest is successful, helpers terminate
feeding of the first brood when the second fledges, and begin contributing to
the care of the latter (Langen and
Vehrencamp, 1999). Unfortunately, for the other species of
cooperative breeders there are only anecdotal descriptions of division of
labor during multiple brooding.
The principal reason, I suggest, that cooperatively breeding species of
birds have more extensive postfledging offspring care than noncooperative
breeders is precisely because of helper assistance, which lowers the per
capita costs of parenting and sometimes results in more efficient breeding
through division of labor. Breeders can recuperate and renest, while other
group members continue to care for the fledglings until the next brood
requires significant investment, after the eggs have hatched
(Drent and Daan, 1980 ;
Weathers, 1996). Even for the
few cooperatively breeding species that breed only once per season, the
duration of care may be more prolonged than similar noncooperative breeders if
the burden-lightening contributions of helpers allow care providers to
maintain better condition. The period of prolonged offspring provisioning may
result in a reduction of the considerable risks associated with the
acquisition of foraging skills in young birds at negligible costs to the
breeders' fitness.
In addition, offspring may benefit more from prolonged care in cooperative
than in noncooperative breeders for two reasons. First, the cost of extended
parental care to a recipient offspring in terms of any reduced residual
reproductive value of related care providers may be lower on average in
cooperative than in noncooperative breeders. This is because from the
perspective of a recipient offspring in a noncooperatively breeding species,
this cost is in terms of lost full or half siblings (r 
.25),
whereas from the same perspective in a cooperatively breeding species, some of
the care providers (the helpers) are at best full siblings of the recipient
and so this cost via the helpers is in terms of lost nieces and nephews or
less closely related kin (r .25). Second, the offspring in many
noncooperative breeders disperse as soon as they become independent to gain an
advantage at competing for feeding or breeding territories nearby home or, for
migratory species, in the wintering range (e.g.,
Nilsson, 1990 ;
Yoerg, 1998). It appears to
be less advantageous to disperse at an early age in most cooperative breeders
(hence the presence of helpers, which are typically philopatric offspring of
previous broods), so offspring gain nothing by becoming independent
sooner.
Prolonged offspring care in cooperative breeders may not be caused by
inherent differences in the rate of development between them and their
noncooperative relatives, but this does not preclude a subsequent evolutionary
slowing of development in lineages with a long history of cooperative breeding
as a consequence of the availability of extended care. For example,
development may slow to lower the peak power demand of growing offspring,
which in turn lowers the risk of starvation
(Ricklefs, 1984). Prolonged
care by adults may also facilitate evolutionary specialization toward foraging
behavior that requires a long period of development to master, with a
consequence that cooperative breeding becomes obligatory, as may be the case
in some New World jays (Langen,
1996) and the white-winged chough
(Heinsohn, 1991). Finally and
most speculatively, slowing of development may be associated with increased
life span in birds (Ricklefs,
1993). Because attainment of breeding status occurs substantially
later than sexual maturity in most cooperative breeders and mortality is
associated with senescence in some (Brown,
1987 ; Holmes and Austad,
1995 ; Lawton and Lawton,
1986 ; McDonald et al.,
1996), a potential evolutionary consequence of the availability of
extended postfledging care may be a slowing of the maturation rate from
selection to increase the life span.
Cooperative breeding and the duration of offspring care in other
taxa
As in birds, prolonged offspring care is associated with cooperative
breeding in insects (Alexander et al.,
1991). The potential for helpers to extend the period of offspring
care is thought to be an important factor in the evolution of cooperative
breeding in these animals. For example, the advantages provided by a division
of labor in which older immature offspring continue to care for their younger
siblings while their parents undertake production of the next brood may have
facilitated the transition toward eusociality in termites and their relatives,
the cooperatively breeding roaches
(Nalepa, 1994). Cooperative
breeding permits extended offspring dependence even when breeders are at
significant risk of dying because helpers can continue to provide care after
loss of a breeder. The frequent evolution of cooperative breeding in some
groups of social insects may in part have been facilitated by the ability of
such insects to provide prolonged offspring care despite relatively low adult
survivorship (Alexander et al.,
1991 ; Gadagkar,
1990 ; Nonacs,
1991 ; Queller,
1989,
1994).
In mammals, cooperative breeding appears to be associated with species for
which offspring production is inherently costly
(Creel and Creel, 1991 ;
Creel and MacDonald, 1995 ;
Geffen et al., 1996 ;
Moehlman and Hofer, 1997).
Most nourishment to offspring in cooperatively breeding mammals is provided by
the mother in the form of milk ; other group members can only provision
offspring indirectly by providing food to the nursing mother. Unlike insects
and birds, it appears that the contributions of helpers result in shorter
periods of offspring dependence in mammals, at least for those in the order
Carnivora (Creel and Creel,
1991). The period of dependence appears to be shorter because the
lactating mother of the offspring provides more milk to them as a consequence
of the provisioning she receives from the helpers. More milk results in faster
growth of the offspring and therefore earlier independence
(Oftedal and Gittleman, 1989).
There may be fundamental differences in how cooperative breeding affects
offspring care between those animals in which an important form of care such
as food provisioning can only be performed by a parent, and those animals in
which all members of the breeding group can contribute. For mammals that
provide food to weaned young (e.g., canids), it may be worthwhile to examine
how offspring provisioning differs after weaning between cooperatively
breeding species and their noncooperative relatives.
|
ACKNOWLEDGEMENTS |
|---|
I am beholden to the University of California library system, which struggles to maintain its excellence in spite of severe financial constraints. I appreciate the helpful suggestions of the reviewers and those provided by Peter Dunn, Jeffrey Walters, Robert Gibson, Sandra Vehrencamp, Peter Nonacs, Aviva Liebert, Maria Duik-Wasser, and especially Trevor Price. This research was supported by a National Institutes of Health National Research Service Fellowship and some opportune loans from Allan T. Langen.
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REFERENCES |
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