Adoption of Chicks by the Pied Avocet SZABOLCS LENGYEL Department of Evolutionary Zoology and Human Biology, University of Debrecen, 4032 Debrecen, Egyetem tér 1., Hungary E-mail: [email protected] Abstract.—Data on the occurrence and frequency of adoption of chicks by adult Pied Avocets (Recurvirostra avosetta) were collected by monitoring individually color-banded chicks on alkaline lakes in the Kiskunság National Park in central Hungary between 1998 and 2000. Fifty-three adoptions were observed, and 22% of the resighted broods (N = 244) contained on average 1.7 (range 1-6) adopted chicks. Ninety-two chicks, or 13% of the color-banded chicks (N = 697) were adopted. The frequency of adoption was similar among years and was positively related to the number of pairs within a colony. At least 60% of the adoptions occurred in the nesting colonies, whereas adoptions during brood movements or in the brood-rearing areas, as well as brood amalgamations, were rare. More than two-thirds (68%) of the adopted chicks in the colony left the natal brood and joined other broods voluntarily. The remaining adopted chicks were the last to hatch in their own brood and were adopted into another brood after being left behind by their parents. Adults did not behave aggressively toward young alien chicks and always accepted them. Adoption appears to be initiated by chicks in Pied Avocets, and it may be associated with small fitness costs, or may even provide benefits, for the adoptees or the adopting adults. Received 18 September 2001, accepted 14 November 2001. Key words.—Adoption, alloparental care, brood rearing, Pied Avocet, Recurvirostra avosetta, shorebirds, wading birds. Waterbirds 25(1): 109-114, 2002

Alloparental care, the caring for young by adults other than their genetic parents (Riedman 1982; Skutch 1987), has been reported in over 220 bird species (Brown 1987). The most widespread forms of alloparental care are adoption and brood amalgamation, where the adults, besides caring for their genetic young, provide parental care to non-filial young that become members of their family group after hatching. Although adoption is found in species with altricial young, “true” adoptions are more likely in precocial birds (Pierotti 1988), and have been reported to occur in rheas (Rheidae) (Codenotti and Alvarez 1998), grouse (Phasianidae) and wild Turkeys (Meleagris gallopavo) (Maxson 1978; Mills and Rumble 1991), ducks and geese (Anatidae, Anseridae) (reviewed by Eadie et al. 1988), gulls and terns (Laridae) (reviewed by Pierotti and Murphy 1987), and shorebirds Scolopacidae, Charadriidae) (Cooper and Miller 1992; Lanctot et al. 1995). Although adoption has been studied intensively in waterfowl, gulls and terns, adoption in other taxa remains virtually unknown. For example, numerous shorebirds and galliform birds have been reported to adopt chicks (Skutch 1976;

Johnsgard 1981, 1983), however, the mechanisms and conditions of adoption have been studied in only two shorebird species (Cooper and Miller 1992; Lanctot et al. 1995). Here I present data on the occurrence, mechanisms and conditions of adoption of chicks in a colonially nesting shorebird, the Pied Avocet (Recurvirostra avosetta). Individually marked avocet chicks were used to identify cases of adoption and data were collected on the occurrence, formation and frequency of adoptions. METHODS Study Sites and Study Period Fieldwork was conducted on Pied Avocets breeding on alkaline lakes in the Kiskunság National Park (KNP) in central Hungary, near Fülöpszállás (46°40’N, 19°10’E), from 1998 to 2000. Alkaline lakes in this area are shallow (<1 m) water bodies varying in surface area from 2 ha to 500 ha, with bare or sparsely vegetated shorelines and islands. These lakes are natural habitats for avocets in central Europe. In addition, fieldwork was conducted in artificial habitats (a drained fishpond and a reconstructed wetland) because of their importance in avocet nesting. Fieldwork was concentrated in areas of high nesting density. Data collected at six alkaline lakes and two artificial sites are included in this study. Fieldwork was started in early May in 1998 and in midMarch in 1999 and 2000 and ended in mid-July in each year.

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Study Species The Pied Avocet is a middle-sized shorebird breeding mostly in coastal areas in Europe and near alkaline lakes to the east of the Black Sea. Its main breeding habitats are salt marshes, salt evaporating ponds on the coast and large alkaline or saline lakes inland (Cramp and Simmons 1983; Hagemeijer and Blair 1997). Avocets nest in colonies, which often are formed on small islands. The species is monogamous and both parents incubate the eggs and care for the young. The chicks are fully precocial and are able to walk and feed on their own a few hours after hatching. After hatching, parents lead their young from the nesting colony to feeding areas, where adults with young occupy multi-purpose territories. Field Methods Nests were located by searching areas used by avocets for nesting. Every nest was numbered, marked and the expected date of hatching of the eggs was estimated by floating the eggs in hand-warm water. Colonies in which eggs were hatching were searched for young chicks at least once per day and the chicks were considered to belong to the nest in which they were found. Searches were conducted in the early morning, when chicks were more likely to be in the nest than later, during warmer times of the day. Chicks found in a nest were covered with a piece of cloth to keep them warm and to prevent them from leaving the nest while chicks in other nests were examined and marked. Chicks were banded above the tarso-metatarsus with brood-specific combinations of two plastic color-bands and a metal band of the Hungarian Ornithological Society. Chicks within a brood were distinguished by pieces of tape attached to the metal band. In all, 61% of the chicks known to hatch in this study (N = 1,301) were marked and at least one chick was marked in 81% of the broods (N = 367). Almost all chicks were marked within 24 h of hatching. Broods were monitored by regularly locating avocet families near the nesting colony, on brood-leading routes and in the brood-rearing areas. Searches were conducted every two or three days using a telescope to find vigilant adults and to count and identify their chicks. During observations, blinds and a car were used as observation points, which were positioned at a distance from the families to avoid disturbance.

broods). These events involved 92 adopted chicks (13% of the chicks resighted at least once, N = 697 chicks). In 1998, the proportion of broods with at least one adopted chick was 16% (N = 25 resighted broods), 21% in 1999 (N = 116) and 24% in 2000 (N = 103) and the proportions did not differ significantly among years (G-test, n.s.). The proportion of adopted chicks was 10% in 1998 (N = 71 resighted chicks), 11% in 1999 (N = 331) and 17% in 2000 (N = 295), which again was not significantly different among years (G-test, n.s.). Adopting pairs (N = 53) had on average 3.1 ± 1.05 (range: 1-5) chicks before adoption and 4.8 ± 11.43 (range: 3-9) chicks after adoption and, on average, had 1.7 ± 11.16 (range 1–6) adopted chicks. Most adopting pairs had two or three chicks before adoption and more than half of the adopting pairs adopted one chick (Fig. 1). When two chicks were adopted (N = 15 cases), in eleven cases they belonged to different broods, and only in four cases were they from the same brood. When three chicks were adopted (N = 4 cases), the adopted chicks came from two different broods in three cases, and in one

Data Analysis Data from the three years were pooled. However, yearly variation was examined where appropriate. Parametric tests were used only if the data met the assumptions of such tests; otherwise, non-parametric tests were used. Means ± 1 SD are reported.

RESULTS The Frequency of Adoption Adoption was found in 53 broods (22% of broods resighted at least once, N = 244

Figure 1. Distribution of adoption events (N = 53) by the number of resident chicks (chicks in the brood of the adopting pair before adoption) and by the number of chicks adopted by the pair in the Pied Avocet. Most adopting pairs had two or three chicks before adoption and most pairs adopted one chick only. Pied Avocet broods were monitored at alkaline lakes of the Kiskunság National Park in south-central Hungary between 1998 and 2000.

HOW DO AVOCETS ADOPT ALIEN CHICKS?

case all three adopted chicks were from the same brood. In the four cases when more than three chicks were adopted, the adopted chicks in each case came from three different broods. The Occurrence of Adoption in Space and Time Fifty-nine chicks (64% of adopted chicks, N = 92) were adopted in the nesting colony, whereas ten chicks (11%) were adopted during brood movements (Table 1). The adoption of 20 chicks (22%) occurred most likely in the colony, but it could have also taken place during brood movement. Finally, adoptions in the feeding areas involved the transfer of three chicks (3%). Adoption in the Nesting Colony All pairs that adopted chicks (N = 53) had nested in colonies in which at least ten clutches hatched (N = 12) and adoptions were observed in all but one of these colonies. The one exception was a colony in which 15 broods hatched highly asynchronously. The number of adoption events was

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positively correlated with the number of nests in the colonies (Spearman r12 = 0.85, N = 14 colonies with more than three pairs that hatched chicks, P < 0.01). However, there was no correlation between the proportion of adopting pairs and synchrony within a colony as measured by the standard deviation of the hatching dates from the mean colony hatch date (Spearman r12 = 0.15, N = 14, n.s.). The asynchronous hatching of eggs within a nest played an important role in the formation of adoptions in nesting colonies. Two or more days passed between the hatching of the first chick and the hatching of the last chick in 64% of the nests (N = 364 nests with known hatching periods). When hatching of the chicks within a brood took a long time, the first-hatched (or second- or thirdhatched) chicks sometimes left the natal brood before their last-hatching sibling was ready to leave the nest. Twenty-two chicks that became adopted in the colony (37% of all chicks adopted in the colony, N = 59) were the first-hatched chicks in their natal brood and 14 (24%) chicks were second- or third-hatched chicks (Table 1). These chicks probably left their incubating parents to feed

Table 1. Number of Pied Avocet chicks adopted under various conditions during the three years of the study. Motivation was “voluntary” for chicks that left their natal brood before the natal brood departed the nesting island, and “forced” for those that were either left behind by their parents or whose siblings had died and were abandoned by their parents. Adoption events with location indicated as “Colony or brood movement” most likely occurred in the nesting colony, but the exact location could not be determined. Location of adoption Nesting colony

Motivation of the adopted chick Voluntary Forced

First-hatched Second or third-hatched Left behind Siblings died

22 14 14 3 6

First-, second- or thirdhatched Left behind

10

Unknown Colony or brood movement

Voluntary Forced Unknown

Brood movement

Feeding areas

Voluntary Forced Unknown Voluntary Forced

Number of chicks

Siblings died

Siblings died Total

7 3 2 6 2 2 1 92

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with other chicks and left the nesting colony in the foster brood before their natal brood was ready to leave. Two direct observations showed that older chicks joined the other broods when the foster adults departed with their young from the nesting island. The foster adults were not observed to behave aggressively toward young chicks in these or any other adoption events during this study. In other cases, parents left the nesting colony before the last-hatching chick was able to leave the nest. Fourteen chicks that were adopted in the colony (24% of all chicks adopted in the colony, N = 59) were the last chicks to hatch in their nests and were left behind by their parents (Table 1). Three other chicks (5%) became adopted after their siblings died from attacks by gulls and terns (Table 1). These chicks attempted to join other nests or broods, and sometimes were adopted by neighboring adults incubating eggs. The adults initially pecked at the alien chicks, but later accepted them. In one case, chicks abandoned by their parents were seen adopted by a pair halfway through incubation and on three occasions by pairs whose eggs were close to hatching. I never observed incubating parents abandoning their eggs after adopting an alien chick. In at least three cases, the chick gained temporary entry to nests with eggs, and was eventually accepted by other adults with chicks. Chicks gaining adoption into nests died in, or near, the nest on six occasions, most likely from starvation. In summary, 68% of the chicks adopted in the colony (N = 53 chicks of known motivation) left their own brood “voluntarily”, whereas 32% of the chicks gained adoption into other broods because they were forced to do so if they were to survive. A significantly higher proportion of the adopted chicks were voluntary adoptees than what could be expected based on a random 50-50% distribution of chicks between the two categories (Yates’ corrected χ21 = 6.02, P < 0.05).

ments in six adoption events. When pairs moved their broods from the nesting colony to feeding sites, adults usually showed aggression to other adults with chicks. During these fights the chicks from the two broods sometimes intermingled, which could have led to adoption. Such a scenario was inferred from resightings in six cases. Resighting observations suggested that only three adoptions occurred after the pairs with chicks occupied territories in the brood-rearing areas. Although pairs usually defended their territory from other adults and chicks, sometimes chicks wandering from one territory into another were not chased back by the owner of the territory. In such cases, the neighboring pair could adopt the chicks. Brood Amalgamation Brood amalgamation, when chicks from several broods merge and are cared for by several adults, was observed twice. Both cases resulted from unusual circumstances. First, the predation of hatching eggs in a colony by a European Badger (Meles meles) presumably caused some adult avocets to abandon their young. Five chicks from three broods formed an amalgamated brood, which was attended by up to five adults. Six chicks from three other broods temporarily joined the amalgamated brood on several occasions. Second, landscape morphology restricted the movements of broods to a narrow passage between lakebeds used by broods as feeding sites. Pairs and their broods crossing this area frequently became involved in territorial fights during which the chicks freely intermingled. Some adults apparently abandoned their young, which led on one occasion to the formation of an amalgamated brood of ten chicks from four broods, attended by four adults. DISCUSSION

Adoption During Brood Movements and In the Brood-rearing Areas Ten chicks (11% of the adopted chicks, N = 92) were adopted during brood move-

Adoption was frequent; 22% of the pairs adopted chicks and 13% of the chicks were adopted. The frequency of adoption did not differ in the three study years. There are no

HOW DO AVOCETS ADOPT ALIEN CHICKS?

published data on the frequency of adoption in other colonies of Pied Avocets, only that it does occur (Cadbury and Olney 1978; Cramp and Simmons 1983). In American Avocets (Recurvirostra Americana), 20% of the pairs adopted chicks in one year and 32% in another year (Lengyel et al. 1998). These observations suggest that adoption is a normal behavior in both the Pied Avocet and in closely related avocet species. Most adoptions occurred in the nesting colony, before or at the departure of broods to the feeding areas. It is, therefore, not surprising that more adoptions occurred in larger colonies, in which there is a greater chance of several broods hatching at about the same time. Asynchronous hatching of the eggs within a clutch played a substantial role in the formation of adoptions in the nesting colony. Earliest-hatching chicks left their natal brood voluntarily, before their parents and siblings departed from the nesting island. The exact cause of departure by these chicks remains unclear. However, physiological demands, such as the urge to feed, are likely to be important in the departure of these chicks, most of which were at over 24 hours old. On the other hand, asynchronous hatching often resulted in late-hatching chicks being left behind by their parents. These chicks became adopted into other broods after the departure of the natal brood from the nesting colony. Adoptions also occurred during broodleading and in the feeding areas. However, these events were less frequent and chicks adopted in these cases were frequently those whose siblings had died. Finally, special circumstances also led to the formation of brood amalgamations; however, these events were rare. Several hypotheses can explain why chicks leave their own brood and why parents adopt chicks. The facts that most chicks appear to leave their natal brood voluntarily and that adopting pairs are frequent suggest that adoption incurs small fitness costs or provides benefits to either the adoptees or the adopters, or both. First, adoption can increase the survival of the chicks through diluting the risks of predation in larger groups

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(Munro and Bedard 1977; Kehoe 1989; Pierotti 1991; Lanctot et al. 1995; Nastase and Sherry 1997). Second, larger broods may be better at detecting predators or at defending themselves against predators (Kear 1970; Gorman and Milne 1972). Third, thermoregulation may be more efficient in larger groups of chicks than in smaller ones (Gorman and Milne 1972; Evans 1984; Carter and Hobson 1988; Kehoe 1989). Finally, brood size may be related to the dominance of the brood or the quality of the adopting parents, and larger broods may occupy better feeding territories than can smaller broods (Black and Owen 1989; Kehoe 1989; Williams 1994; Loonen et al. 1999). In conclusion, adults accept young chicks, probably because the costs of tolerating alien chicks in the brood are small. Also, adoption can provide benefits for either the adopted chick, the adopting parent, or both. Further observations and experiments are necessary to distinguish among these hypotheses to explain adoption in avocets and in shorebirds in general. ACKNOWLEDGMENTS The Kiskunság National Park and the Hungarian Ornithological Society provided field permits. The help of K. Lippai, B. Lontay, Cs. Pigniczki, A. Soltész, and O. Somogyvári in the field is greatly appreciated. Field equipment was provided by C. Richard Tracy and the Biological Resources Research Center at the Department of Biology at the University of Nevada, Reno, U.S.A. The study was financially supported by two grants (F 26394 and F 30403) from the National Base Programs for Scientific Research (OTKA) of Hungary. LITERATURE CITED Black, J. M. and M. Owen. 1989. Agonistic behaviour in Barnacle Goose flocks: assessment, investment and reproductive success. Animal Behaviour 37: 199-209. Brown, J. L. 1987. Helping and Communal Breeding in Birds. Princeton University Press, Princeton, New Jersey. Cadbury, C. J. and Olney, P. J. S. 1978. Avocet population dynamics in England. British Birds 78: 102-121. Carter, H. R. and K. A. Hobson. 1988. Creching behavior of Brandt’s cormorant chicks. Condor 90: 395400. Codenotti, T. L. and F. Alvarez. 1998. Adoption of unrelated young by Greater Rheas. Journal of Field Ornithology 69: 58-65. Cooper, J. M. and E. H. Miller. 1992. Brood amalgamation and alloparental care in the least sandpiper,

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Lengyel, Sz., J. A. Robinson and L. W. Oring. 1998. Chick recognition in American Avocets: a chick-exchange study. Auk 115: 490-494. Loonen, M. J. J. E., L. W. Bruinzeel, J. M. Black and R. H. Drent. 1999. The benefit of large broods in barnacle geese: a study using natural and experimental manipulations. Journal of Animal Ecology 68: 753768. Munro, J. and J. Bedard. 1977. Gull predation and créching behaviour in the common eider. Journal of Animal Ecology 46: 799-810. Nastase, A. J. and D. A. Sherry. 1997. Effect of brood mixing on location and survivorship of juvenile Canada geese. Animal Behaviour 54: 503-507. Pierotti, R. and E. C. Murphy. 1987. Intergenerational conflicts in gulls. Animal Behaviour 35: 435-444. Pierotti, R. 1988. Intergenerational conflicts in species of birds with precocial offspring. Proceedings of the XIX International Ornithological Congress: 1265-1274. Pierotti, R. 1991. Infanticide versus adoption: an intergenerational conflict. American Naturalist 138: 1140-1158. Riedman, M. L. 1982. The evolution of alloparental care and adoption in mammals and birds. Quarterly Reviews of Biology, 57: 405-435. Skutch, A. F. 1976. Parent Birds and their Young. University of Texas Press, Austin, Texas. Skutch, A. F. 1987. Helpers at Birds’ Nests. University of Iowa Press, Ames, Iowa. Williams, T. D. 1994. Adoption in a precocial species, the lesser snow goose: Intergenerational conflict, altruism or a mutually beneficial strategy? Animal Behaviour 47: 101-107.