The Auk 126(2):371 375, 2009 The American Ornithologists’ Union, 2009. Printed in USA.
GROUP TERRITORIALITY AS A FORM OF COOPERATIVE BREEDING IN THE FLIGHTLESS KAGU (RHYNOCHETOS JUBATUS) OF NEW CALEDONIA J ÖRN THEUERK AUF,1,5 S OPHIE ROUYS , 2,3 J EAN M ARC M ÉRIOT,4 1
AND
ROMAN G ULA1
Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland; 2 Conservation Research New Caledonia, B.P. 2549, 98846 Nouméa Cedex, New Caledonia; 3 LIVE, Université de la Nouvelle-Calédonie, B.P. 4477, 98847 Nouméa Cedex; and 4 Parc Provincial de la Rivière Bleue, Direction de l’Environnement, Province Sud, New Caledonia
Abstract.—Birds that live in family groups and cooperatively defend the family’s territory are currently recognized as cooperative breeders only if helpers assist with chick rearing. We observed breeding Kagus (Rhynochetos jubatus) and video-monitored nests to determine whether help with feeding or family size affected their reproductive success. During , h of nest monitoring, helpers never provided parents or chicks with food. The reproductive success of families increased with group size nonetheless. Family size affected breeding success more than habitat-related parameters. Nonbreeding Kagus reacted to playback calls as often as breeding birds did. Observations of territorial fights gave additional evidence that nonbreeding group members help defend the family’s territory and can, therefore, improve reproductive success. Our results suggest that cooperative territory-defense was the most important factor that increased the breeding success of Kagus. We propose that group territoriality should be considered a form of cooperative breeding. Received May , accepted December . Key words: communal breeding, group territoriality, Kagu, Rhynochetos jubatus, territorial behavior, territory-defense.
La territorialité de groupe, une forme de reproduction coopérative chez un oiseau inapte au vol (Rhynochetos jubatus) Résumé.—A l’heure actuelle, les oiseaux qui vivent en groupes familiaux et dont la famille entière participe à la défense du territoire commun ne sont reconnus en tant que reproducteurs coopératifs que si des membres de la fratrie aident au nourrissage des poussins. Nous avons suivi des nids de Rhynochetos jubatus par vidéosurveillance et observations directes afin de déterminer si la taille de la famille ou l’aide au nourrissage des poussins affectait le succès de reproduction. Sur plus de heures de vidéosurveillance de nids, aucun oiseau non reproducteur n’a apporté de nourriture aux parents ou aux poussins. Le succès de reproduction augmentait cependant avec la taille du groupe familial. La taille des familles avait une influence plus importante sur le succès de reproduction que les paramètres d’habitat. Les individus non reproducteurs réagissaient aussi souvent que le couple reproducteur à la repasse de chants de R. jubatus. Des observations de combats territoriaux ont permis de confirmer que les membres non reproducteurs de la famille participent à la défense du territoire et peuvent par là même accroître le succès de reproduction. Nos résultats indiquent que la défense commune du territoire était le facteur décisif pour l’augmentation du succès de reproduction. Nous proposons d’inclure la territorialité de groupe à la définition de la reproduction coopérative. Cooperative breeding in birds is particularly common in the Australasian region (Russell ), though it is relatively uncommon in precocial birds (Cockburn ). Cooperative-breeding groups usually consist of one or several breeding pairs and nonbreeding birds that often help feed the chicks (Emlen , Cockburn ). Nonbreeding group members that are related to the breeding birds are usually offspring that delay dispersal and breeding and stay in their parents’ territory. Late dispersers often have a survival advantage over those that leave early (Ekman
et al. , Griesser et al. ), because they stand a chance of inheriting a high-quality territory from their parents (Ekman et al. a, b; Kokko and Ekman ) and can have higher reproductive success over the long term (Ekman et al. ). Delayed dispersal of young sometimes brings a direct benefit to the parents, if the older siblings help with feeding chicks; the benefit can also be indirect, if offspring survival is higher (Crick , Koenig et al. , Blackmore and Heinsohn , Doerr et al. , Cockburn et al. ).
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In New Caledonia, the endemic, precocial Kagu (Rhynochetos jubatus) and two endemic parakeet species are the only species suggested as being cooperative breeders (Létocart and Salas , Cockburn , Theuerkauf et al. ). Kagus live in family groups that consist of a breeding pair and their offspring of various ages. A family usually rears only one chick per year, and both parents take shifts in incubating the egg. Kagus reach sexual maturity at three years but can delay dispersal for as long as years (J. Theuerkauf et al. unpubl. data). Létocart and Salas () stated that nonbreeding Kagus take an active role in rearing their siblings, but they did not specify how these family members help. Here, we use data on Kagu reproduction to highlight an aspect of cooperative breeding that has been overlooked. We used playback calls, filmed nests with surveillance cameras, and observed Kagus to quantify the contribution of helpers to territory-defense and to assess the influence of family size on reproductive success. Our objectives were to investigate () whether nonbreeding family members provide the incubating parents or the chick with food and () the effect that family group size and habitat-related factors have on breeding success. We show that parents had a higher breeding success when nonbreeding family members helped in territory-defense. M ETHODS From to , we monitored breeding attempts of Kagu families living in the Rivière Bleue Provincial Park (n–`S, n–`E). We banded Kagus to estimate the total number of Kagus in the families and fitted of them with harnessmounted radiotransmitters (Sirtrack, Havelock North, New Zealand). To avoid counting individuals that had left their parents’ territory, we estimated the family size as the maximum number of birds that we saw together during daytime or on night roosts or that had reacted simultaneously to the playback (Létocart ) of Kagu calls (family size ranged between and Kagus in the studied families). We found Kagu nests by locating radiotracked Kagus at night, when they were either roosting or on a nest. We filmed breeding attempts of eight families during incubation and breeding attempts of four families with chicks before fledging (chicks leave the nest when they are – days old). We filmed nests continuously using infrared illuminator cameras (Sony /p CCD image sensors) and Electret mini microphones with integrated SMD amplifiers (Henri Electronic, Germany). The footage was recorded on VHS recorders (Panasonic NV-HV from –) or digital video recorders (Archos and Archos in –), which were – m away from the nest. Our recording method was similar to that described in Pierce and Pobprasert (). Kagus feed their chick and brood it at night for about two months after fledging (Létocart and Salas ). To assess whether chicks survived the fledging period, we regularly located radiotracked parents; a chick survived the fledging period if we observed it alive two months after fledging. We assessed the annual breeding success of each family by a combination of three variables: () the number of eggs laid, () the number of chicks hatched, and () the number of chicks that survived the fledging period. If a female laid a replacement egg after the first egg failed to hatch, we excluded the replacement egg from the analyses. Kagus react to playback of Kagu calls, and all family members that hear the calls usually come to investigate—and, potentially,
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defend—the territory. To quantify this defense behavior for each family, we compared the proportion of helpers lured and captured using playback with the proportion of helpers in the family. We caught Kagus in nets that we placed in vegetation between them and the playback speaker. Only Kagus that ran into the net, apparently defending their territory, were caught; those that investigated the call without running had time to see and avoid the net. To see whether nonbreeding family members helped by feeding parents or chicks, we watched footage taken at nests. Because reproductive success is likely to be associated with habitat factors, we evaluated the quality of a family’s territory using two parameters: home-range size and population density. We created MCPs (minimum convex polygons) from radio locations of breeding Kagus (– locations individual−) and calculated the home-range size of a family as the mean of the MCPs of each parent (homerange size ranged between . and . km in the studied families). We calculated population density as the number of all Kagus banded in a family, divided by the family’s home-range size (population density ranged between and Kagus km− in the studied families). We used linear regression models and Akaike’s information criterion (AIC) to assess which of the three parameters (family size, population density, and home-range size) most influenced reproductive success and ranked them by Akaike weights (Burnham and Anderson ). Family size, population density, and home-range size are not independent of one another. However, we expected that family size would be the parameter least related, and home-range size the parameter most related, to habitat quality. We hypothesized that if habitat quality is the main factor influencing breeding success, family size should be ranked below the more habitat-related parameters in regression models. R ESULTS Nonbreeding family members visited the nest on occasions ( times during incubation, times while a chick was present) in three of the eight families during , h of video-monitoring. Parents were the only birds providing food to the chick in all feeding events that we recorded by video-monitoring. During incubation (, h of video-monitoring), a yearling that was chased by other family members sought protection from the mother on four occasions. On one occasion, a nonbreeding Kagu arrived with the breeding male and left with the female after the parents changed their incubating shift. On seven occasions, the incubating parent displayed nonaggressively to the nonbreeding family member. A parent responded once to the nonbreeding family member’s visit by leaving the nest, but on another occasion the parent did not react to the helper’s presence. There were three visits of nonbreeding family members to the nest during a parent’s absence; in all cases, the helper looked briefly at the egg before leaving. During the two to four days after hatching and before fledging ( h of video-monitoring), parents displayed aggressively to the nonbreeding family member on four occasions but did not react to four other visits. On three occasions, a nonbreeding family member arrived at the nest in the absence of the parents but paid little attention to the chick. On two occasions, a yearling begged for food that the parents intended to give to the chick, but the yearling was not fed.
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TABLE 1. “Family size” was the most important parameter influencing nest survival (fledglings family−1 year−1) in linear models ranked by Akaike weights (w), whereas the mainly habitat-related parameter “home-range size” played a more important role for chicks that survived the first two months after fledging (n 38 breeding attempts of Kagus in the Rivière Bleue Park, 2003–2008). Rank 1 2 3 4 5 6 FIG. 1. The mean annual numbers of hatchlings (medium-gray columns with thin inverse-regression line) and chicks (dark-gray columns with bold inverse-regression line) that survived the two-month fledging period increased with increasing Kagu family size, whereas the mean annual number of eggs laid (white columns) did not depend on family size (n 38 breeding attempts in 11 Kagu families in 2003–2008 in the Rivière Bleue Park, New Caledonia; samples sizes above the bars).
Although the number of eggs produced per year in a family did not depend on the size of the family group (y . − ./x, P ., rS ., n breeding attempts), the number of fledglings (y . − ./x, P ., rS .) and the number of juveniles that survived the fledging period (y . − ./x, P ., rS .) increased with family size (Fig. ). Nevertheless, breeding success did not increase for family sizes greater than four. One family abandoned their fertile egg after several days of territorial fights with neighboring families. Two days before they abandoned the egg, the female, assisted by the single nonbreeding family member, chased an unknown Kagu out of their territory. The next day, we saw the female while she was fighting alone with an unknown Kagu that dominated the fight. Following that fight, the pair no longer incubated the egg during the day, and they abandoned the nest three days later. We observed a nonbreeding family member feeding a chick in only of the families, but this family was not video-monitored. In another family, we observed adult helpers chasing a yearling of the same family over the course of several days. The incubating parents did not act aggressively toward the yearling, which sometimes sought their protection. At that time, the family consisted of the breeding pair, three adult helpers, the yearling, and the chick. In nine families, the percentage of nonbreeding family members caught by playback was o % (% confidence interval), which was similar to the overall percentage of nonbreeding family members ( o %). Family size was the highest-ranking factor influencing nest survival (sum of Akaike weights .), followed by population density (.) and home-range size (.; Table ). For the rate of juvenile birds surviving the fledging period, the most important factor was home-range size (sum of Akaike weights .), followed by population density (.) and family size (.).
1 2 3 4 5 6
Parameters in model
$AICc
AICc
0.00 1.39 2.89 3.39
−63.35 −61.96 −60.46 −59.96
3.40 4.94
−59.95 −58.41
0.318 0.304
0.00 0.09
−58.11 −58.02
0.293
0.16
−57.95
0.034 0.030 0.020
4.47 4.71 5.54
−53.64 −53.40 −52.57
w
Before fledging Family size 0.458 Family size, population density 0.228 Population density 0.108 Family size, home-range size, 0.084 population density Home-range size 0.083 Home-range size, population 0.039 density After fledging Home-range size Home-range size, population density Family size, home-range size, population density Family size, population density Family size Population density
D ISCUSSION We found that reproductive success in Kagus was positively associated with family size, and we suggest that additional nonbreeders caused the increase. An alternative hypothesis is that the greater success of some breeders results in larger families and that the number of nonbreeders is a consequence, not a cause, of greater reproductive success. However, the multimodel regression analyses showed that family size was a more important factor than population density or home-range size, which makes it unlikely that habitat quality alone explains breeding success. Helpers only rarely fed chicks, but helpers are known to defend chicks (Hunt ) and the family territory as much as parents do. Our observation that a breeding pair with only one helper abandoned a fertile egg after several days of territorial fights suggests that the help of nonbreeding family members in defending the family’s territory is crucial to successful breeding when population density is high. By preventing intrusions into the territory, nonbreeding birds enable the parents to concentrate on caring for the egg or the chick. Innes and Johnston () showed that helpers reduced predation on broods in White-throated Magpie-jay (Calocitta formosa). Because Kagus have no predators, except for introduced stray dogs (Hunt et al. ), a major benefit of nonbreeding Kagus to their parents is reduction of nesting failure related to competition with neighboring Kagu families. Birds with long offspringdependence frequently have helpers, because parents can breed again while helpers care for the last brood (Langen ). However, Kagus usually have only one brood per year, which may explain the rarity of feeding by other group members. In Whitewinged Chough (Corcorax melanorhamphos), helpers increase
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their effort when chicks grow older (Boland et al. ). Therefore, we may have underestimated the rate of feeding by helpers because we used video-monitoring only during the nest stage. However, the main reproductive failure of small families was clearly during incubation (see Fig. ), the period when help in feeding was lacking and family size appeared to be the most important parameter associated with nesting success. White-winged Choughs and Carrion Crows (Corvus corone) are cooperative breeders, and their reproductive success increases with group size (Heinsohn , Canestrari et al. b). Similarly, reproductive success in Kagu families increased with one helper and was highest when there were at least two helpers. We observed that in a family of five Kagus, however, nonbreeding group members chased the yearling of the family daily while the parents were brooding. This may indicate a conflict between helpers in large families, as has been found in other species (Ekman et al. , Griesser et al. ). The observation that the yearling requested and obtained protection from its incubating parents also suggests that although large families are beneficial to parents, they also increase competition among siblings for territory inheritance. Cockburn (:) defined cooperative breeding as “the case in which there is some evidence that more than % of nests in one or more populations are attended by more than two birds.” According to this definition, our data do not provide evidence of cooperative breeding in Kagus. Group defense of territories is usually not considered cooperative breeding. For example, Chowchillas (Orthonyx spaldingii) cooperatively defend home ranges, but, because they do not help with chick rearing, Jansen () concluded that Chowchillas are not cooperative breeders. However, Gayou () considered group territoriality an evolutionarily early form of cooperative breeding. We propose that the distinction between help with territory-defense and help with feeding is irrelevant; what matters is the effect that cooperation of helpers has on breeding success. We suggest that the helping strategy of Kagus reflects an adaptive response to strong territorial competition. Cockburn () previously postulated that cooperative breeding is not just a simple dichotomy between cooperative societies with delayed dispersal and those formed via recruitment of unrelated individuals into coalitions. We propose expanding the definition of “cooperative breeding” to include territory-defense by nonbreeding helpers, because this behavior increases the reproductive success of the breeding pair. Nonbreeding group members do not necessarily increase reproductive success in all group-territorial species (e.g., Jansen ), but neither do helpers in all cooperative species. For example, Australian Magpies (Gymnorhina tibicen) are cooperative breeders in Tasmania (Dow ), but in New Zealand their reproductive success does not depend on group size, despite defense of common territories (Veltman ). The effect of group territoriality on reproductive success may depend on environmental conditions, especially the availability of food, given that helpers can adjust their provisioning in response to the availability of resources (Canestrari et al. a). Our results suggest that group territoriality leads to higher reproductive success in Kagus, especially in high-density situations, and should, therefore, be considered a form of cooperative breeding.
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This study was part of the research project “Impact of introduced mammals and habitat loss on endemic birds of New Caledonia” carried out by Conservation Research New Caledonia in collaboration with the Direction de l’Environnement (Province Sud, New Caledonia) and financed by the Polish Ministry of Science and Higher Education (grant PF ), Conservation des Espèces et Populations Animales (France), La Fondation Nature et Découvertes (France), Loro Parque Fundación (Spain), Fonds für bedrohte Papageien—Zoologische Gesellschaft für Arten- und Populationsschutz (Germany), and a doctoral grant from Province Sud (to S.R.). We thank M. Broersen, C. Chatreau, P. de Pous, D. Dingemans, S. Duijns, B. Michielsen, E. Minnema, L. Nijdam, H. Theuerkauf, J. van Dijk, M. van Opijnen, J. Wardenaar, N. Petit, and many others for their help during field work; and G. R. Hunt, D. B. McDonald, and two anonymous reviewers for useful comments. LITERATURE CITED Blackmore, C. J., and R. Heinsohn. . Reproductive success and helper effects in the cooperatively breeding Grey-crowned Babbler. Journal of Zoology :–. Boland, C. R. J., R. Heinsohn, and A. Cockburn. . Experimental manipulation of brood reduction and parental care in cooperatively breeding White-winged Choughs. Journal of Animal Ecology :–. Burnham, K. P., and D. R. Anderson. . Model Selection and Multimodel Inference: A Practical Information-theoretic Approach, nd ed. Springer-Verlag, New York. Canestrari, D., E. Chiarati, J. M. Marcos, J. Ekman, and V. Baglione. a. Helpers but not breeders adjust provisioning effort to year-round territory resource availability in Carrion Crows. Animal Behaviour :–. Canestrari, D., J. M. Marcos, and V. Baglione. b. Reproductive success increases with group size in cooperative Carrion Crows, Corvus corone corone. Animal Behaviour :–. Cockburn, A. . Evolution of helping behavior in cooperatively breeding birds. Annual Review of Ecology and Systematics :–. Cockburn, A. . Prevalence of different modes of parental care in birds. Proceedings of the Royal Society of London, Series B :–. Cockburn, A., R. A. Sims, H. L. Osmond, D. J. Green, M. C. Double, and R. A. Mulder. . Can we measure the benefits of help in cooperatively breeding birds: The case of Superb Fairy-wrens Malurus cyaneus? Journal of Animal Ecology : –. Crick, H. Q. P. . Load-lightening in cooperatively breeding birds and the cost of reproduction. Ibis :–. Doerr, E. D., V. A. J. Doerr, and R. J. Safran. . Integrating delayed dispersal into broader concepts of social group formation. Behavioural Processes :–. Dow, D. D. . Communally breeding Australian birds with an analysis of distributional and environmental factors. Emu : –.
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