«Ellen Kalmbach1), Pascal van der Aa & Jan Komdeur (Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, PO ...»
Adoption as a gosling strategy to obtain better
parental care? Experimental evidence for gosling
choice and age-dependency of adoption
in greylag geese
Ellen Kalmbach1), Pascal van der Aa & Jan Komdeur
(Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of
Groningen, PO Box 14, 9750 AA Haren, The Netherlands)
(Accepted: 25 July 2005)
Adoptions of unrelated young by successful breeders are a form of alloparental care which
has been observed in many species of geese. Depending on costs and beneﬁts to the par- ents, adoptions might represent an inter-generational conﬂict or a mutually beneﬁcial strategy.
Although most studies of wild populations suggest beneﬁts of large brood sizes, incidental observations mostly report aggressive behaviour of parents towards lone goslings. No stud- ies have investigated mechanisms and behaviour during adoptions in order to test whether adoptions are driven by parents or goslings. To test whether goslings might use adoption as a strategy to obtain better parental care, we carried out an experiment where lone greylag goose (Anser anser) goslings could choose between a dominant and a subordinate foster family. In a second experiment we also tested whether adoption was age-dependent. Except for one case, all lone goslings (N = 16) chose the dominant family. Parents showed very little aggression towards lone goslings at three days after hatch, but aggression increased until 9 days and remained high thereafter. At the same time as aggression increased, the chance of success- ful adoption decreased. In the ﬁrst ﬁve weeks of life, goslings which had been adopted were no further away from parents than original goslings during grazing. These results show that goslings might choose foster families according to dominance. The fact that with increasing gosling age parents are less willing to adopt could be due to improved individual recogni- tion and reﬂect decreasing beneﬁts of gaining an additional family member. More detailed studies on state-dependent costs and beneﬁts of adoptions are required to determine whether adoptions in geese represent conﬂict or mutualism, and why this changes with gosling age.
1) Corresponding author’s current address: Max Planek Institute for Demographic
Research, Konrad-Zuse-Strasse 1, 18057 Rostock, Germany; e-mail address:
firstname.lastname@example.org © Koninklijke Brill NV, Leiden, 2005 Behaviour 142, 1515-1533 Also available online - 1516 Kalmbach, van der Aa & Komdeur Keywords: post-hatch brood amalgamation, Anatidae, reproductive error, intra-speciﬁc para- sitism, greylag goose.
Introduction The provisioning of care to young by individuals other than the genetic par- ents is a behaviour that has been described in many animals and is broadly referred to as alloparental care (Riedman, 1982). Although at ﬁrst sight investing resources into non-genetic offspring appears contradictory to the aim of maximising ones genetic contribution to future generations, particularly for cooperative systems it has been shown that alloparents can gain direct and indirect beneﬁts (Clutton-Brock, 2002; Roulin, 2002; Koenig & Dickinson, 2004). Apart from cooperative breeding systems, alloparental care also occurs in other reproductive systems, including those with social monogamy and biparental care (Riedman, 1982). In birds various forms of brood mixing have been described, such as communal crèching, brood amalgamations and adoptions. The term adoption has been used in many different contexts. We deﬁne it as a form of alloparental care where one or several foreign young permanently join another brood, and the parents of the original brood exclusively provide all aspects of parental care to these young (Eadie et al., 1988).
The ﬁtness consequences and adaptiveness of this kind of alloparental care are little studied and understood (Emlen et al., 1991; Kalmbach, in press).
Geese are precocial birds with biparental care and are known to frequently adopt goslings that are not their own, with up to 50% of families containing adopted young (Zicus, 1981; Choudhury et al., 1993; Larsson et al., 1995). In wild populations, adopters appear to be almost exclusively successful breeders who have goslings of their own at the time of adoption (Zicus, 1981;
Williams, 1994; Larsson et al., 1995). This observation has lead to the traditional explanation of adoptions as ‘reproductive error’ due to imprecision of parent-offspring recognition at an early age (Jamieson, 1986; Emlen et al., 1991). Although adoptions are most common during the goslings’ ﬁrst week of life, they have also been observed throughout the whole brood rearing period of two to three months (Prevett & MacInnes, 1980; Choudhury et al., 1993; Williams, 1994). These observations suggest that adoptions can not only be explained by a recognition mistake between parents and goslings, as individual recognition is developed by the age of 10 to 15 days (Ramsay, 1951; Prevett & MacInnes, 1980). If adoptions are adaptive for the goslings 1517 Adoption in greylag geese but gaining additional brood members is costly to parents, they would represent an intergenerational conﬂict (Pierotti, 1988). If, however, parents gain beneﬁts from an increased family size, then adoptions might be mutually beneﬁcial (Williams, 1994; Loonen et al., 1999).
Lazarus & Inglis (1986) have proposed that large broods are not costly to parents with respect to parental investment of which all offspring beneﬁt simultaneously, such as vigilance or brooding behaviour (‘unshared investment’ sensu Lazarus & Inglis, 19861 ). As most of the post-hatch parental care in precocial species falls into the category of ‘unshared investment’, large broods should not be more costly than small broods for parents in such species. In fact, very few studies have actually tried to identify costs of raising large families in geese (Kalmbach, in press). Evidence from observational studies generally shows that larger families are more dominant, which leads to better access to high quality feeding areas, and that gosling growth and condition is enhanced, while no negative effects on adult survival or future reproduction are found (Seddon & Nudds, 1994; Williams et al., 1994;
Lepage et al., 1998; Loonen et al., 1999). Although non-breeders have been found to have a higher return rate than breeders (Raveling, 1981; Petersen, 1992; Prop et al., 2004), amongst emperor goose Chen canagicus females those with larger families had higher survival than those with small families (Petersen, 1992). Of the three studies to date which have carried out brood size manipulations in geese, two have found strong evidence for a causal relationship between family size and social dominance, as well as gosling growth (Lepage et al., 1998; Loonen et al., 1999). Also, both parents and juveniles gain beneﬁts from large families and long family association on the wintering grounds (Black & Owen, 1989a, b). It appears that on the whole large broods are more beneﬁcial than costly to goose parents and their genetic offspring. Beside these indirect beneﬁts of adoption via enlarged family size, it has been suggested that adoptions might provide direct beneﬁts 1 In the original paper by Lazarus & Inglis (1986) ‘unshared investment’ is deﬁned as an act of parental care which is directed at the brood as a whole and of which therefore all offspring beneﬁt equally (unshared = everyone gets all of the investment, not only a share).
‘Shared investment’ is deﬁned as an act of parental care which beneﬁts individual offspring to a different degree, up to the case of monopolization by one offspring, such as delivery of food items. Lazarus & Inglis (1986) argue that the costs of ‘unshared investment’ do not vary with brood size, while costs of ‘shared investment’ increase with increasing brood size.
1518 Kalmbach, van der Aa & Komdeur of predation avoidance through predation dilution and the selﬁsh herd effect (Hamilton, 1971; Eadie & Lumsden, 1985; Nastase & Sherry, 1997).
These results suggest indeed that adoption might be a beneﬁcial strategy of parents to increase their family size, particularly when they can do so without incurring the costs of laying and incubating extra eggs. From the gosling’s perspective, it has traditionally been assumed that adoption occurs as a salvage strategy after having lost its parents (Choudhury et al., 1993; Williams, 1994; Nastase & Sherry, 1997). However, from our own and other researchers’ observations, it is often the case that original parents are still alive and present in the local feeding group, particularly in cases when adoptees are very young (K. Kotrschal, J. Prop, M.J.J.E. Loonen, pers.
comm.). We suggest that adoption could also be an active strategy of goslings to obtain better parental care or higher social status (Pierotti, 1988).
In this study, we carried out behavioural experiments with a semi-captive greylag goose Anser anser population to test three hypotheses about the role of parents and goslings in adoptions. (1) If adoption is a strategy by goslings to obtain better parental care, goslings should be able to discriminate between parents of different quality, and, if given the choice, choose the higher quality family. (2) If an increase in family size entails mainly beneﬁts and not costs, parents should be basically willing to adopt. (3) If adoption is a strategy by parents to decrease predation risk of their genetic offspring, we expect to see a difference in the distances between original and adopted goslings to the parents. Through aggressive or threatening behaviour goslings might be kept at the periphery of the group and predation risk could be skewed towards fostered young, thereby providing protection for original young (Öst & Bäck, 2003).
Methods Study population and clutch manipulation The study was carried out in the breeding seasons (March-August) of 2003 and 2004 with a captive population of greylag geese. The geese are kept on
0.5 ha area of grassland, bushes and water pools near the Biological Centre of the University of Groningen (The Netherlands). The population was started in 1992 with eggs that were collected from the wild. Wing feathers are clipped every year during moult to prevent geese from ﬂying away. The 1519 Adoption in greylag geese ﬂock consisted of 76 (40 males, 36 females) and 63 (33 males, 30 females) adults and several juveniles in 2003 and 2004, respectively. All geese were individually marked with numbered aluminium leg rings and uniquely coded plastic neck rings, which are legible from a distance. From the start of the breeding season, the whole area was checked every day for new nests and eggs.
To avoid any potential bias in our experiments due to genetic relatedness of goslings and parents, we prevented all eggs that were laid by the captive geese from developing through thorough shaking, and replaced them with eggs from a wild population. The wild eggs were collected by members of the Dutch Forestry Commission under a licensed control scheme for local goose populations, and obtained by us under licence from the Ministry for Agriculture, Environment and Fisheries (licence number FF/75A/2003/048).
Wild eggs were initially kept in an incubator at 37.5◦ C and around 55% humidity and grouped by the stage of development, which was estimated by inspection with a lamp.
Shortly before hatching in 2003, groups of ten eggs were formed, of which three each were put into two nests, while the other four were hatched in the incubator. After hatching, the incubator goslings were kept with a pair of failed breeders in a smaller enclosure where a heating lamp was present as well as an outdoor part. The adults were kept with the goslings to avoid imprinting of goslings on humans. Although the female did not brood the goslings, the adults did not show aggression towards the goslings, and even defended the goslings against approaching humans. Through this procedure we obtained ‘twinned’ nests in the ﬁeld, with broods of three goslings each hatched on the same day, while four more goslings of the same age were present in the foster-enclosure. In 2004, groups of 12 eggs were formed, of which three each were put into three nests in the ﬁeld, and the remaining three hatched in the incubator and were kept with the foster parents. The fact that in 2004 groups of 3 twinned families existed is of no further importance to the experiments described in the present paper. Nests in the ﬁeld were ‘twinned’ according to the original start of incubation, to avoid large differences in the time females had spent incubating within the sets of twinfamilies.
Gosling choice experiment In 2003, we carried out a choice experiment where lone goslings were able to choose between two potential adoption families. For this, we built open cages 1520 Kalmbach, van der Aa & Komdeur Figure 1. Schematic layout of the enclosure used for the gosling choice experiment with position of test gosling and families during testing phase. All separations were made with chicken wire. The separations between compartment C and A and A contained doors where only goslings could pass through (indicated by the dashed line). Those doors were closed before the testing phase, i.e. during the interaction period of the experiment (see text).
in a separate part of the ﬁeld, which contained four compartments (Figure 1).
All separations between the compartments were made of chicken wire and it was possible for all geese to see through the fences. When goslings were two days old, the twinned families were placed in the compartments A and A with some water, and left to get accustomed to the cages and surroundings for a minimum of one hour. Then both families were placed in compartment B, with water and food placed in the middle, while a lone gosling was placed in compartment C with food and water. The lone gosling came from the foster enclosure and was of the same age as the family goslings.
For a minimum of 30 minutes, the two families were left in part B, while the lone gosling was left in part C. All interactions between the two families were scored by two observers to determine which family was more dominant.