Cooperative breeding by Buff-throated Partridge Tetraophasis szechenyii: a case in the Galliformes

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1 DOI /s z ORIGINAL ARTICLE Cooperative breeding by Buff-throated Partridge Tetraophasis szechenyii: a case in the Galliformes Yu Xu Nan Yang Kai Zhang Bisong Yue Jianghong Ran Received: 5 July 2010 / Revised: 2 December 2010 / Accepted: 3 January 2011 Ó Dt. Ornithologen-Gesellschaft e.v Abstract Cooperative breeding is rarely found in the Galliformes. We report a case in Buff-throated Partridge Tetraophasis szechenyii, a sexually monochromatic Galliform species endemic to western China. A total of 68 groups were detected in the breeding seasons, and cooperative breeding was observed to be facultative, with 64.7% (44/68) of pairs having up to three helpers of either sex (but predominantly male). Groups usually remained stable within the breeding season. Sampling revealed that all adult members exhibited behavioral efforts in terms of brooding, vigilance, and territorial display (including calling and fighting), with helpers especially focusing on territorial fighting. No evidence was found to suggest that the presence of helpers significantly enhanced a group s breeding success and productivity compared to unaided pairs. Further studies, particularly intraspecific comparative analyses (for example, between populations or between sites) and those measuring the relatedness between helpers and other group members, are needed to understand the occurrence of cooperative breeding in this species. Keywords Breeding success Cooperative breeding Galliformes Group structure Helping Tetraophasis szechenyii Zusammenfassung Kooperatives Brüten findet sich selten innerhalb der Galliformes. Wir beschreiben einen Fall beim Rostkehl-Keilschwanzhuhn Tetraophasis szechenyii, einer farblich sexual-monomorphen, galliformen Vogelart, die in Westchina endemisch ist. Insgesamt 68 Gruppen wurden in den Brutsaisons nachgewiesen und kooperatives Brüten war bei dieser Art fakultativ, wobei 64,7% (44/68) der Paare bis zu drei Helfer beider Geschlechter hatten (überwiegend allerdings Männchen). In der Regel blieben die Gruppen über die Brutsaison hinweg stabil. Die Untersuchung erbrachte, dass alle alten Mitglieder Aufwand in Form von Brut-, Wachsamkeits- und Territorialverhalten (inklusive Rufen und Kämpfen) zeigten, wobei sich die Helfer speziell auf Territorialkämpfe konzentrierten. Wir fanden keine Hinweise darauf, dass die Anwesenheit von Helfern den Bruterfolg und die Produktivität einer Gruppe im Vergleich zu Paaren ohne Helfer wesentlich verbessert haben könnte. Weitere Studien, die intraspezifische Vergleichs-Analysen (z. B. zwischen Populationen oder zwischen Standorten) durchführen und den Verwandtschaftsgrad zwischen Helfern und anderen Gruppenmitgliedern messen, sind notwendig um das Auftreten von kooperativem Brüten bei dieser Art zu verstehen. Communicated by T. Friedl. Y. Xu and N. Yang contributed equally to this work. Y. Xu N. Yang K. Zhang B. Yue J. Ran (&) College of Life Sciences, Sichuan University, Chengdu , China rjhong-01@163.com Introduction Cooperative breeding is a social system which involves more than two individuals of the same species providing care in rearing young from a single nest or brood (Brown 1987; Stacey and Koenig 1990). The fitness benefits of this system are well documented, including the increased production of genes in future generations (indirect benefits)

2 and/or an enhanced chance of survival or breeding experience (direct benefits), either immediately or in the future (Cockburn 1998; Hatchwell and Komdeur 2000; Dickinson and Hatchwell 2004). Notwithstanding the benefits, cooperative breeding is rare, especially in birds, occurring in only % of documented species (Brown 1987; Stacey and Koenig 1990; Arnold and Owens 1998), and at most in 9% of bird species using phylogenetic inference based on the assumption of biparental care as the default pattern (Cockburn 2006; Hatchwell 2009). In the Galliformes specifically, which is a large and diverse bird group comprising 70 genera and more than 250 species (Madge and McGowan 2002), this behavioral system is even more rare (Arnold and Owens 1998; Ligon and Burt 2004), with likely occurrences limited to hybrids between the White Eared Pheasant Crossoptilon crossoptilon and the Tibetan Eared Pheasant C. harmani (Lu and Zheng 2005), and the Black-breasted Wood Quail Odontophorus leucolaemus (Hale 2006). Interestingly, phylogenetic analysis predicts an absence of cooperative breeding among the Galliformes due to highly precocious young and limited parental care (Ligon and Burt 2004). The Buff-throated Partridge Tetraophasis szechenyii is a medium-sized (length cm, weight 660 1,790 g), sexually monochromatic partridge belonging to the family Phasianidae in the Galliformes (Madge and McGowan 2002; Potapov 2002; Yang et al. 2009). The partridge is endemic to China, mainly occurring in mixed coniferous forests, rhododendron shrubs, oak thickets, alpine meadows, and rocky ravines at high elevation (3,350 4,600 m) in southeast Tibet, south Qinghai, west Sichuan, and northwest Yunnan (MacKinnon and Phillipps 2000; Madge and McGowan 2002; Lu 2006). Previous surveys of the partridge have suggested a monogamous or polygynous mating system (Liu and Ci 1993; Jiacuo 1998; Potapov 2002; Lu 2006), but the results of our investigation challenge these findings. Here, we describe cooperative breeding within this species, documenting group structure, individual disappearance, and turnover within groups, trends in individual behavioral efforts, and breeding success and productivity. Methods Study site This study was conducted on 340 ha near a monastery and sacred mountain in Pamuling ( N E),Yajiang County, Ganzi Tibetan Autonomous Prefecture, Sichuan, China, with elevation ranging between 3,900 and 4,200 m a.s.l. The site is characterized by a series of old coniferous forests, oak thickets, rhododendron shrubs, and meadows (see more details in Xu et al. 2008, 2010). Fieldwork The Buff-throated Partridges at the study site were very tame, as they have always been supplied with food by the monks from the monastery and by visitors to the sacred mountain due to their sanctity in the local culture. We captured partridges by funnel-traps baited with rice in either the early or late breeding season. In total, 35 individuals were captured over 4 years (10, 9, 11, and 5 in 2006, 2007, 2008, and 2009, respectively) and fitted with metal or colored tarsus bands. Seven marked individuals disappeared or died soon after marking, or the bands dropped off. Nine adults (2 in 2006, 2 in 2008, and 5 in 2009) were equipped with necklace-transmitters (model RI-2D; weight 18.5 g, frequency MHz, lifespan 36 months; Holohil Systems, Carp, ON, Canada), of which two dropped off within 1 month after placement. In addition to bands and transmitters, groups were recognizable by the locations of territories and unique plumage characteristics among individual birds (breeding season only). The partridges were surveyed (using radio-tracking or playbacks) by repeatedly searching the study site at least once a month from March to October between 2006 and 2009; in most months there were multiple surveys. Once a group was detected, its identity was determined using binoculars and followed from a distance while recording the general behavior attributes. For groups with helpers, the social status of adult members was determined by their spatial distribution and interactions while foraging for food (e.g., pecking, chasing, and escaping behavior). Along the high-to-low dominance hierarchy, males and females were described as # 1, # 2, # 3, etc., and $ 1, $ 2, $ 3, etc., respectively. The # 1 and $ 1, which usually kept in close contact with each other while foraging, were viewed as the breeding pair, and the others were viewed as helpers. For some cooperative groups, we made additional behavioral observations on incubating activities and posthatching foraging activities, focusing on brooding (protecting or warming chicks by covering with abdomens and wings), vigilance (raising heads for attention and alertness), and territorial display (announcing territories and driving intruders away, including calling and fighting), which reflect contributions to cooperation (Sherman 1977; Stacey and Koenig 1990; Weathers et al. 1990; Theuerkauf et al. 2009a). (Cooperative provisioning to young, indeed, is the best evidence for the occurrence of cooperative breeding, but unfortunately this behavior was not recorded, although we did detect it). For each nest, there were at least two whole-day observations, and on other days, at least two other 2-h continuous samplings recording identity and duration of the incubating individual. To record foraging activities, we used the randomly continuous behavior

3 recording technique with sampling periods lasting at least 30 min (i.e., recording all occurrences of behavior and their durations; Martin and Bateson 1994). A behavior was not recorded if its duration was\20 s each time. All behavioral observations were made using binoculars at a distance of 10 m. Data analyses Analyses were restricted to groups that were detected multiple times throughout the whole breeding season; groups detected \3 times or detected only in a specific period were regarded as floaters and excluded from the analyses. A group was considered to be stable if its size and structure (excluding additions from the current year s brood) remained unchanged during the majority of surveys throughout a breeding season. However, a long survey gap over winter (5 months) made it difficult to determine group stability in terms of size and structure across years, especially for unmarked groups. For groups in which adult members disappeared early in the breeding season and then regrouped with other groups, only the compositions later in the breeding season were used in the analyses. If a group was never observed regrouping after the recorded disappearance, we included the disappeared individuals in analyses only if the group bred successfully before these individuals were lost to the study. Disappearance of an individual was treated as either a death or dispersal out of the study area, and regrouping behavior was labeled as turnover restricted within the study population. It was easy to determine individuals exhibiting these behaviors for a group during the breeding season, regardless of whether they were marked or not, because multiple and regular surveys enabled the recognition of individuals by the locations of group territories and the unique plumage characteristics of individual birds. The rates of disappearance and turnover across a breeding season were calculated by dividing the number of individuals that exhibited these behaviors by the total number of individuals in the population. However, this was difficult to establish over the winter period because of the survey gap. As such, for each winter period we restricted our calculation to marked individuals by dividing the number of marked individuals that exhibited these behaviors by the total number of individuals marked in the population. We used Fisher s exact test to examine whether the frequencies of winter disappearance and turnover in different social identities (i.e., male, female, and young) were in proportion to the numbers appearing in the population. We determined breeding success as a group successfully rearing at least one young to 2 months of age, at which time they finished molting into complete juvenile plumage and had developed most of the agility of their parents. At this stage young birds have reached a high level of potential to pass genes onto the next generation. We defined productivity of a group as the total number of young successfully reared to the juvenile plumage stage by the group per breeding season. Breeding success, rather than breeding attempts (e.g., nesting success, and hatching success), was used in the study because the latter was undetermined in some groups. Chi-square tests for independence were applied to determine if the proportion of breeding success differed between unaided pairs and groups with at least one helper. Due to extremely small sampling sizes in groups consisting of four (n = 2) and five (n = 1) individuals, we did not examine the correlation between productivity and group size and instead used the Mann Whitney U test to analyze whether productivity differed between unaided pairs and groups with at least one helper. In terms of behavioral observations on foraging activity, we calculated frequencies of occurrence (times/ h) and percentages of time (%) spent in brooding, vigilance, and territorial display behaviors for each sampling period. One-way analysis of variance (when variables were normal) and Kruskal Wallis tests (when they were not) were used to determine if frequencies and percentages of time spent in these behaviors were significantly different among individuals; if differences existed, least significant difference multiple comparisons were used to determine which individuals differed. For variables which were not normal, rank cases were performed prior to the comparisons. All of the analyses were performed using SPSS ver (SPSS 2009). P \ 0.05 was interpreted as being statistically significant, and means are given throughout as ± standard error, unless otherwise stated. Results Group structure, individual disappearance and turnover In total, 68 groups (18 in 2006, 16 in 2007, 17 in 2008, and 17 in 2009) were recorded. The mean size of the groups (excluding the current year s young) was 2.81 ± 0.09 (n = 68), with 64.7% (44/68) of pairs having up to three helpers. Both sexes acted as helpers, but there was a predominant bias towards males (8.3:1). Groups, by occupying exclusive territories, were usually stable within the breeding season, with low rates of individual disappearance [1.9% (1/53) in 2006, 4.2% (2/48) in 2007, 7.5% (4/53) in 2008, and 8.3% (4/48) in 2009] and turnover [0% (0/53) in 2006, 2.1% (1/48) in 2007, 1.9% (1/53) in 2008, and 4.2% (2/48) in 2009]. In contrast, the frequency of individual disappearance [0% (0/4) in 2006,

4 Fig. 1 Frequency and percentage of time [mean ± standard error (SE)] spent in brooding (white bars), vigilance (gray bars), and territorial display (black bars) for two groups of the Buffthroated Partridge (Tetraophasis szechenyii) in Pamuling, Sichuan, China, The number in the top right corner of each sub-figure indicates the group number. Brooding occurred during the first month of the chicks life (n = 45-h observations from 18 continuous behavior samplings for group 1, and n = 17-h observations from six continuous behavior samplings for group 2); vigilance and territorial display occurred in the whole breeding season (n = 121-h observations from 53 continuous behavior samplings for group 1, and n = 94-h observations from 39 continuous behavior samplings for group 2). #1 indicates the breeding male. Significance for multiple comparisons is shown above the bars: *P \ 0.05, **P \ 0.01, ***P \ % (3/9) in 2007, and 7.7% (1/13) in 2008] and turnover [75% (3/4) in 2006, 11.1% (1/9) in 2007, and 23.1% (3/13) in 2008] increased in winter. In the study reported here, both winter disappearance and turnover were proportionally most frequent among young [54.5% (6/11); Fisher s exact test P \ 0.01]. Behavioral contributions Females incubated eggs exclusively, while males spent the majority of their time either foraging or guarding around the nest (observations on seven cooperative groups comprised of one female and multiple males). During posthatching foraging, all adult members exhibited brooding, vigilance, and territorial behavior, yet their contributions towards specific behaviors appeared unpredictable (Fig. 1), with the exception of the helpers especially focusing on fighting behavior (n = 9 observations from two of these seven groups) in the form of territorial display. Breeding males were only recorded exhibiting fighting behavior twice, and both times followed the defeat of male helpers to a rival male. Females never participated in fighting behavior. Breeding success and productivity In total, 29.4% (20/68) of groups bred successfully, with each group having only a single brood. The proportion of breeding success in groups with at least one helper (34.1%, 15/44) was higher than that in unaided pairs (20.8%, 5/24), but the trend was not significant (chi-square test v 2 = 1.315, df = 1, P = 0.252). A similar result was also found for productivity (Mann Whitney U Z =-0.692, P = 0.489; Fig. 2). Discussion The results of previous surveys suggested Buff-throated Partridges to be monogamous or polygynous (Liu and Ci 1993; Jiacuo 1998; Potapov 2002; Lu 2006). It should be argued, however, whether the polygyny is a cooperative breeding system with female helpers to the extent that the breeding status of additional females is not well known. In this study, a facultative cooperative breeding system with heavily male-biased helping was observed in Buff-throated Partridges, with 64.7% of pairs having up to three helpers

5 Given that precocity does not favor cooperative breeding on phylogeny (Ligon and Burt 2004), understanding the occurrence of cooperative breeding in the Buff-throated Partridge is meaningful, especially in the context of habitat constraints or life history. To examine this, further studies aimed at conducting intraspecific comparative-analyses (e.g., between populations or between sites) are recommended. In addition, a genetic analysis that measures relatedness between group members using DNA fingerprinting techniques could provide information critical in identifying the extent of benefits helpers gain by joining a cooperative breeding group (e.g., Theuerkauf et al. 2009b). Fig. 2 Productivity (mean ± SE) between unaided pairs (n = 5) and groups with at least one helper (n = 15) for Buff-throated Partridge groups in Pamuling, Sichuan, China, of either sex (but predominantly male). The high level of group stability observed during the breeding season supports the presence of a stable cooperative display within the population, while frequent disappearance and turnover of group members across years may be contributed to multiple factors, such as adverse conditions during the winter and drive for breeding independently. Based on our sampling results, helpers exhibited efforts behaviorally in terms of brooding, vigilance, and territorial display, including calling and fighting, but they also predominately engaged in territorial fighting more often than the breeding pair. These features of cooperative breeding by the Buffthroated Partridge in our study have been documented in most cooperative breeding bird species (Stacey and Koenig 1990; Cockburn 1998; Ligon and Burt 2004). We did not find that the presence of helpers in a cooperative breeding group significantly enhanced that group s breeding success and productivity, so helpers were less likely to gain the indirect fitness benefits (i.e., increased number of their genes in future generations). Helping may derive from increased direct fitness, such as increased survival and enhanced breeding experiences (Cockburn 1998; Hatchwell and Komdeur 2000; Dickinson and Hatchwell 2004). It is also possible that helpers shared direct parentage of broods as, although we defined the most behaviorally dominant male and female as the breeding pair, the possibility that individuals behaviorally considered as helpers were in fact parents of at least part of the broods cannot be dismissed. It should be noted that our sample size was small, which may limit our understanding of the system. Additionally, we cannot be sure that the results were not influenced by repeated measures of groups across years, despite group composition frequently changing between years. Acknowledgments We thank the Yajiang Forestry Bureau and Pamuling monastery for their permission and the support given to this field work. We thank Pengfei Yu and Liang Dou for assistance in the field work and Jason Scott (University of Georgia), Hugh A. Ford (University of New England) and anonymous reviewers for useful comments and advice during the revisions of the manuscript. The study complies with the current laws of China. References Arnold KE, Owens IPF (1998) Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc R Soc Lond B 265: Brown JL (1987) Helping and communal breeding in birds. Ecology and evolution. Princeton University Press, Princeton Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29: Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc B 273(1592): doi: /rspb Dickinson JL, Hatchwell BJ (2004) Fitness consequences of helping. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp Hale AM (2006) Group living in the Black-breasted Wood-quail and the use of playbacks as a survey technique. Condor 108: Hatchwell BJ (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil Trans R Soc B 364(1533): doi: /rstb Hatchwell BJ, Komdeur J (2000) Ecological constraints, life history traits and the evolution of cooperative breeding. Anim Behav 59: Jiacuo GM (1998) Pheasant grouse in Baimaxueshan (White Horse Snow Mountains). Chin Wild 20:34 Ligon JD, Burt DB (2004) Evolutionary origins. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 5 34 Liu SC, Ci R (1993) Tetraophasis szechenyii of Tibet. Chin Wild 15:19 21 Lu TC (2006) Buff-throated partridge Tetraophasis szechenyii. In: Lei FM, Lu TC (eds) China endemic birds. Science Press, Beijing, pp Lu X, Zheng GM (2005) Cooperative young-caring behaviour in a hybrid population of White and Tibetan Eared-pheasants in Tibet. Ardea 93:17 24 MacKinnon J, Phillipps K (2000) A field guide to the birds of China. Oxford University Press, Oxford

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