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Relatedness and the evolution of conspecific brood parasitism: parameterizing a model with data for a precocial species
ANIMAL BEHAVIOUR, 2004, 67, 673e679 doi:10.1016/j.anbehav.2003.08.009
Relatedness and the evolution of conspecific brood parasitism: parameterizing a model with data for a precocial species ¨ YS A ¨ H AN N U P O
Finnish Game and Fisheries Research Institute, Joensuu Game and Fisheries Research (Received 25 November 2002; initial acceptance 7 February 2003; final acceptance 4 August 2003; MS. number: 7547R)
Conspecific brood parasitism (CBP) is a common reproductive tactic in several animal taxa, especially in precocial birds. It has been suggested that hosteparasite relatedness can facilitate the evolution of CBP. A recent model showed that the existence and accuracy of the kin recognition system is crucial for this to occur. I used field data to parameterize the model for the common goldeneye, Bucephala clangula, a precocial species in which CBP frequently occurs and in which a recent finding of nonrandom hosteparasite relatedness has been interpreted to support the idea that relatedness and kin selection influence CBP. It turned out that possibilities to detect brood parasitism and accurately discriminate between kin and nonkin parasites are negligible in the species. The empirically parameterized model exercise revealed that relatedness and kin selection are unlikely explanations of CBP in the species. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Conspecific brood parasitism is an alternative reproductive tactic in which a female lays eggs in the nest of a conspecific female that takes care of incubation and the young. Several hypotheses have been put forward to explain the evolution of this reproductive tactic (Andersson 1984; Eadie et al. 1988; Petrie & Møller 1991; Sayler 1992). The subject in general has received considerable theoretical attention (e.g. Rubenstein 1982; Andersson 1984, 2001; Bulmer 1984; Eadie & Fryxell 1992; Zink 2000; Broom & Ruxton 2002; Lo´pez-Sepulcre & Kokko 2002). In particular, the role of kin selection in the evolution of conspecific brood parasitism has recently been in focus (Zink 2000; Andersson 2001; Lo´pez-Sepulcre & Kokko 2002). The models by Zink (2000), Andersson (2001) and Lo´pez-Sepulcre & Kokko (2002) differ in several important aspects and assumptions (see also Lyon & Eadie 2000) and, because of that, the models also reach diverging conclusions about the influence of kin selection on the evolution of conspecific brood parasitism. In brief, although one of the main findings of Zink (2000) was that relatedness should not promote the evolution of conspecific brood parasitism, Andersson’s (2001) model suggested that it can. One of the basic differences between Zink (2000) and Andersson (2001) was that their models assumed different levels of cost from parasitism. In Zink’s model, the direct cost for a parasitized host was assumed Correspondence: H. Po¨ysa¨, Finnish Game and Fisheries Research Institute, Joensuu Game and Fisheries Research, Kauppakatu 18-20, FIN-80100 Joensuu, Finland (email: hannu.poysa@rktl.fi). 0003e3472/03/$30.00/0
to be large (i.e. a host clutch size is reduced by the exact number of parasitic eggs laid in the nest), but in Andersson’s model, the direct costs were assumed to be small or moderate. In general, if direct costs of parasitism are large, hosteparasite relatedness will not make parasitism advantageous and, hence, it is better to parasitize an unrelated host (see also Andersson 2001, page 607). While taking into account the different approaches of Zink (2000) and Andersson (2001) concerning the costs of parasitism, Lo´pez-Sepulcre & Kokko (2002) focused on the role of kin recognition that was assumed to be perfect in Andersson’s (2001) model. Their model revealed that the existence and accuracy of a kin recognition system is crucial to determine whether parasitism should be directed towards relatives or nonrelatives. If parasitism is costly to the host, and the host cannot accurately discriminate between related and unrelated parasites, kinship will not promote the evolution of conspecific brood parasitism. The above discussion demonstrates how crucial it is to build models on biologically realistic assumptions and parameter values to understand the influence of relatedness and kin selection on the evolution of conspecific brood parasitism. Lo´pez-Sepulcre & Kokko’s (2002) model made a valuable contribution to the subject, because it was based on biologically realistic assumptions and identified the crucial importance of the accuracy of kin recognition, a parameter that has not been empirically measured so far. The other critical model parameter that has been difficult to estimate with field data is the cost of parasitism (but see Eadie & Fryxell 1992). We need
673 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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empirical studies to get biologically realistic estimates of the critical model parameters for different species and reproductive strategies. In this paper, I use field data to parameterize Lo´pezSepulcre & Kokko’s (2002) model for the common goldeneye, Bucephala clangula, a precocial hole-nesting species in which conspecific brood parasitism occurs frequently and has been intensively studied (review in Eadie et al. 1995; see also Po¨ysa¨ 1999; Andersson & ˚ hlund 2000). By doing that, I assessed the plausibility of A relatedness and kin selection in explaining brood parasitism in the species. Andersson & A˚hlund (2000) found in a Swedish common goldeneye population that hosts and the primary parasite were more closely related than females in random pairs. They suggested that relatedness and kin discrimination, achieved by recognition of birth nestmates, influence conspecific brood parasitism in the species. In the present study, I focused on the kin recognition system, especially on the possibilities of hosts detecting parasitism in the first place. I also estimated the other model parameters, including the costs of parasitism, by using long-term field data from a Finnish common goldeneye population (Po¨ysa¨ 1999).
THE MODEL Details of the derivation of the full model can be found in Lo´pez-Sepulcre & Kokko (2002). The model parameters are as follows (see Table 1, Lo´pez-Sepulcre & Kokko 2002): Co Z number of eggs laid by a nonparasitic female in a nest without parasitism; Cp Z number of eggs laid by a parasitic female in the host’s nest; Ch Z number of eggs laid by a nonparasitic female when parasitized; p(C) Z proportion of eggs that give young surviving to fledging age; r Z coefficient of genetic relatedness between host and parasite; Ao Z probability of accepting eggs laid by a nonrelative (0%Ao %1); Ar Z probability of accepting eggs laid by a relative (0 % Ar % 1) in the host’s nest. I focused on a submodel addressing a case in which kin recognition is not necessarily perfect and parasitism is costly. In such a case, relatedness will favour brood parasitism if the following equations are satisfied simultaneously (equations 9 and 12 in Lo´pez-Sepulcre & Kokko 2002): r>
Co pðCo ÞCh pðCh þCp Þ Cp pðCh þCp Þ
ð1Þ
and Ar =Ao >
Cp pðCh þCp Þ Cp pðCh þCp Þþr½Ch pðCh þCp ÞCo pðCo Þ
ð2Þ
If there are fitness costs from parasitism, equation (1) specifies the degree of relatedness between host and parasite that must be exceeded before accepting parasitic eggs from a kin is advantageous. Equation (2) in turn specifies a threshold value for the accuracy of kin recognition, Ar/Ao, so that relatedness could promote conspecific brood parasitism; this happens only if related eggs are sufficiently more likely to be accepted than nonkin eggs, i.e. Ar/Ao exceeds the threshold (Lo´pez-
Sepulcre & Kokko 2002). These two quantities, r and Ar/Ao, are under consideration when exploring the parameterized model in the present study. DATA All data are from a common goldeneye population (Intsila¨) in which conspecific brood parasitism and other aspects of the breeding ecology of the species have been ¨ ysa¨ studied intensively since 1992 (Milonoff et al. 1995; Po ¨ ysa¨ et al. 1997a, 1999, 2001b; Po¨ysa¨ 1999; Po¨ysa¨ & Po 2002); data are from 1992e2002 if not otherwise specified. Especially Po¨ysa¨ (1999) and Po¨ysa¨ & Po¨ysa¨ (2002) are referred to for description of the study area and for general methods used in the gathering of nesting data. Most common goldeneye females breed in nestboxes that are available in excess in the area. Most data are from individually known females (ringed and wing tagged; licence from the Finnish Museum of Natural History, University of Helsinki); if data from more than 1 year were available for a given female, I included only one, randomly selected year in the calculations for that female. In the following I explain the data for each of the parameters in the model, except r and Ar, whose possible values are under consideration when exploring the parameterized model.
Clutch Size: Co, Cp and Ch I included all nesting attempts that proceeded to hatching and nest exodus and for which I succeeded in measuring all the eggs; deserted and predated (partially or totally) clutches were not included. I also estimated the start of incubation in each nest as exactly as possible and excluded those nests for which I knew that parasitic eggs were laid after incubation had started. Because in these nests the parasitic eggs would not hatch at all (i.e. incubation time too short; hatched ducklings leave the nest 24e36 h after hatching, Eadie et al. 1995), the cost of parasitism to the host is exceptionally high, although the host will face only an indirect fitness cost if the eggs are laid by a relative. Exclusion of these nests only makes my analysis more conservative. Width and length of all eggs in the clutches were measured, and weights of the eggs were estimated using the formulae developed by Rohwer (1988) for waterfowl. Based on the within-clutch variation (Euclidean distance) of these three egg characteristics, I identified parasitized and nonparasitized nests with a method developed by and explained in Eadie (1989) and later explained, tested and used in Po¨ysa¨ (1999) and Po¨ysa¨ et al. (2001a). If egg size is strongly heritable, the method used to identify parasitized nests might fail to recognize nests parasitized by relatives. Hence, in the present data, some of the clutches that were identified as nonparasitized might in fact have been parasitized by relatives. This seems unlikely, however. First, mean size of clutches that were identified as nonparasitized was 7.0, but that of clutches identified as parasitized was 11.7. If some of the nonparasitized clutches were in fact parasitized, it would mean that host clutch size was, on
¨ YSA ¨ : RELATEDNESS AND BROOD PARASITISM PO
average, about five eggs, an exceptionally small clutch for common goldeneyes (e.g. Eadie et al. 1995). Second, Andersson & A˚hlund (2001) identified parasitized and nonparasitized nests based on protein fingerprinting, a technique that also identifies nests parasitized by close relatives. In their data (Table 4), the mean size of nonparasitized clutches was 7.8, i.e. very close to that in the present study, and the mean number of host eggs in parasitized clutches was 7.9. Hence, I conclude that the method used to identify parasitized and nonparasitized clutches did not bias the data. Mean G SD size of nonparasitized clutches was 7:0 G 1:8 (N Z 15) and of parasitized clutches 11:7 G 2:9 (N Z 31). There is no evidence in the common goldeneye that hosts would decrease their own clutch size in response to parasitism (Sayler 1992; see also Andersson 2001, page 610), so I assumed that Co ZCh Z7, a typical clutch size of nonparasitized nests in the species (Eadie et al. 1995). A direct measure for Cp is not available from the present population. Based on data in Table 4 (H, hatched clutches that were parasitized) of Andersson & A˚hlund (2001), I calculated that the mean number of parasitic eggs per parasitizing female was 2.2 (N ¼ 8); therefore I assumed that Cp ¼ 2:2. In reality, some nests may be parasitized by more than one female (i.e. mean size of parasitized clutches was 11.7) but the costs of parasitism are not strongly dependent on clutch size.
From Eggs to Fledged Young: p(C ) In the case of the common goldeneye, the proportion of eggs that give young surviving to fledging age is a product of three components: the proportion of eggs that hatch ( p(H)), the proportion of hatched ducklings that leave the nest ( p(L)) and the proportion of ducklings leaving the nest that survive until fledging ( p(F)). Because common goldeneye broods frequently change lake soon after nest exodus (Eriksson 1978, 1979; Po¨ysa¨ & Virtanen 1994; Wayland & McNicol 1994), it was impossible to get data for duckling survival for all the broods that left the nest; therefore, sample size was smaller for the brood phase than for the nest phase. Brood mortality in goldeneyes is highest during the first week after nest exodus (Savard et al. 1991; Milonoff et al. 1995; Po¨ysa¨ et al. 1997a), and mortality rate during the first week is a good predictor of mortality rate after the first week until the age of 40 days (Po¨ysa¨ et al. 1997a; see also Po¨ysa¨ & Milonoff 1999). Also, the duration of maternal care depends on prior brood survival in the common goldeneye, and many females desert the brood within the first 2 weeks after nest exodus ¨ ysa¨ et al. 1997a; Po¨ysa¨ & Milonoff 1999). (Po¨ysa¨ 1992; Po Therefore, to get as large and unbiased a data set as possible, I estimated the proportion of fledged young by using broods that I was able to follow individually until the end of the first week after nest exodus. The proportions explained above showed varying responses to clutch or brood size: p(H) was not significantly associated with clutch size (Spearman rank correlation: rS ¼ 0:198, N ¼ 46, NS; range of clutch size 4e16), p(L) decreased with increasing number of hatched
ducklings (rS ¼ 0:382, N ¼ 46, P!0:01; range of the number of hatched ducklings 4e16), and there was no association between p(F) and brood size (rS ¼ 0:008, N ¼ 29, NS; range of brood size 3e16). Andersson & Eriksson (1982) showed that almost all eggs hatched, regardless of clutch size, in successful common goldeneye nests. They concluded that addition of parasitic eggs during the host’s laying period should not markedly reduce hatching success, i.e. p(H) should be independent of clutch size. I am not aware of common goldeneye studies in which the relation between p(L) and the number of hatched ducklings has been examined. However, the negative relation between p(L) and the number of hatched ducklings is biologically realistic. At nest departure, the female is calling for the ducklings outside the nest cavity and the ducklings jump one at a time out from the nest (Eadie et al. 1995). Hence, because the strength-demanding nest departure depends on each duckling’s own condition, and because it may take longer for a larger brood to leave the nest (in Sire´n’s 1952 data of five broods with 4, 5, 6, 9 and 9 ducklings, the departure of the young took 40, 105, 95, 86 and 150 s, respectively), making the nest departure exposed to disturbance for a longer period, one or more of the last ducklings of a large brood may not get out from the nest cavity. Sire´n (1956) described cases in which the female abandoned live ducklings in the nestbox and led away the ducklings that had jumped out. As to the lack of association between p(F) and brood size, observational and experimental results from common goldeneye populations have consistently shown that p(F) is independent of brood size (Milonoff & Paananen 1993; Milonoff et al. 1995, 1998; Po¨ysa¨ et al. 1997a). Andersson & Eriksson (1982) reported that p(F) was a negative function of brood size (but see Milonoff et al. 1995), but Eadie & Fryxell (1992) reported that p(F) was a positive function of brood size in the closely related Barrow’s goldeneye, B. islandica. In sum, the present data did not show strong dependence of p(H), p(L) and p(F) on clutch or brood size, so I decided to use mean values of the proportions, as follows: nonparasitized nests: pðHÞ ¼ 0:961, N ¼ 15; pðLÞ ¼ 1:0, N ¼ 15; pðFÞ ¼ 0:700, N ¼ 12; parasitized nests: pðHÞ ¼ 0:928, N ¼ 31; pðLÞ ¼ 0:988, N ¼ 31; pðFÞ ¼ 0:683, N ¼ 17. These proportions are independent (p(H) versus p(L): Spearman rank correction: rS ¼ 0:064, N ¼ 46, NS; p(H) versus p(F): rS ¼ 0:131, N ¼ 29, NS; p(L) versus p(F): rS ¼ 0:095, N ¼ 29, NS). Therefore, the proportion of eggs that give young surviving to fledging age, p(C), can be calculated as the product of the three proportions, resulting in the following parameter estimates: nonparasitized nests: pðCo Þ ¼ 0:673; parasitized nests: pðCh þ Cp Þ ¼ 0:626.
Accuracy of Kin Recognition: Ar/Ao Common goldeneye females do not defend the nest during the egg-laying period (Eadie et al. 1995). Recognition and rejection or removal of parasitic eggs is also unlikely in common goldeneyes. For example, Andersson &
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Eriksson (1982) experimentally added several parasitic eggs to the nests of common goldeneyes and found no evidence of egg eviction from the nests. They also suggested that identification and eviction of eggs laid by other females may usually be impossible because of the deep and dark nest cavity. Similarly, Milonoff & Paananen (1993) experimentally added eggs from other females in some common goldeneye nests and found that hatching success in these nests did not decrease, implying indirectly that the recipient females did not discriminate against the strange eggs. Hence, the only biologically realistic possibility for the host to detect and reject a nonkin potential parasite is when the host herself visits the nest for egg laying (i.e. the host could prevent the parasite entering the nest). In general, the intervals between eggs are about 1.3e2 days (Eadie et al. 1995). Similarly, Andersson & ˚ hlund’s (2000) video recordings revealed that hosts A during the laying period usually visit the nest only every other day. As Lo´pez-Sepulcre & Kokko (2002, page 218) noted, the value of Ar/Ao summarizes both the effects of kin recognition (i.e. whether Ar > Ao ) and the detection of brood parasitism per se (the absolute value of Ao). Although I do not have data to estimate Ar and Ao directly and separately, I was able to estimate the probability that a host could detect and reject parasitic laying as follows. Related to an ongoing field experiment of conspecific brood parasitism in the common goldeneye (H. Po¨ysa¨, unpublished data), I frequently visited the nestboxes during the laying phase in 1999e2002. During each visit, I recorded whether a female was in the nestbox or whether a female left the nestbox when I approached it. I included only nests that proceeded to incubation (i.e. I was sure that a nest had a host), and there were 68 such nests in all. For each nest, I included only visits after the first egg had been laid and before the incubation had started. Mean G SD number of visits per nest was 5:6G2:9 and the mean length of the period over which the visits were distributed was 8:3G4:1 days per nest. In all, I made 379 such visits to the nests between 0700 and 2100 hours, and I saw a female in the nestbox or the female left the nestbox when I approached it in 33 of the 379 cases. Most of the visits were made between 1100 and 1600 hours (53.8%) and fewer between 0700 and 1100 hours (20.8%) and 1600 and 2100 hours (25.3%). However, the proportion of the visits when a female was in the nestbox did not differ between the three periods (chisquare test: c22 ¼ 3:48, NS). Furthermore, on 22 visits, I recognized a newly laid egg (one of the eggs was much warmer than the other eggs in the clutch; I interpreted that the egg had been laid within the last 2 h before my visit); 10 of these eggs were laid between 0700 and 1100 hours, 10 between 1100 and 1600 hours and two between 1600 and 2100 hours, i.e. egg laying occurred throughout the day. I conclude that my visits to the nestboxes provide a biologically sound way to measure the probability of a host being in the nestbox if a parasitic female tries to enter it for egg laying. These figures can be used to estimate the probability that a host female in general can detect and reject parasitic laying in the common
goldeneye (33=379 ¼ 0:087; this figure is probably an overestimate, because some of the females I saw in the nestboxes may have been laying parasites). The estimated probability is low but not exceptional, considering the biological facts we know about the laying behaviour of common goldeneye females. I used this probability to approximate Ao as follows: Ao ¼ 1 0:087 ¼ 0:913. Even though this measure does not make a difference between nonrelative and relative eggs, it gives the approximate minimum probability for accepting a nonrelative egg, i.e. the ‘true’ value of Ao should be between 0.913 and 1. This is because in common goldeneyes we can assume that a parasitic egg is always accepted if parasitism is not detected (i.e. the host is not in the nest). Using the minimum value of 0.913 for Ao and assuming perfect kin recognition make the model exercise most conservative. Finally, as in the original model (Lo´pez-Sepulcre & Kokko 2002, page 220), I assume that parasites have the choice of finding unrelated females’ nests. This is a realistic assumption in common goldeneyes, because, even though nest site fidelity and female natal philopatry are high in the species (Dow & Fredga 1983; Po¨ysa¨ et al. 1997b; Ruusila et al. 2001), most of the nesting females do not have relatives breeding at the same time in the area (Ruusila et al. 2000). Furthermore, within the same season, a given parasitic female may lay in nests several kilometres apart (Andersson & A˚hlund 2000; A˚hlund & Andersson 2001; Po¨ysa¨ 2003). This evidence means that, in general, the likelihood of being parasitized by a relative should not be higher than that of being parasitized by a nonrelative.
RESULTS If hosts rarely detect brood parasitism, Ao is near 1, and Ar/Ao cannot be high because 0 % Ar % 1 (Lo´pez-Sepulcre & Kokko 2002). In the present common goldeneye population, Ao was estimated to be 0.913. Hence, if we assume perfect kin recognition (i.e. Ar ¼ 1), Ar/Ao has a maximum value of 1.095. Perfect kin recognition is probably unrealistic in common goldeneyes, but I focus on it to make my conclusions about the role of the kin selection hypothesis in explaining conspecific brood parasitism in the species as conservative as possible. The empirically estimated maximum value of Ar/Ao means that, in the present common goldeneye population, close relatedness does not enhance conspecific brood parasitism. Even assuming perfect kin recognition, the range of relatedness, r, where both equations (1) and (2) are fulfilled is narrow (0:239 ! r ! 0:364; Fig. 1, area between the vertical dashed lines). At small values of r, brood parasitism between kin is not favoured because hosts are not selected to accept costly parasitism from too remotely related parasites. At large values of r, parasites are not selected to target related hosts, because they suffer from indirect costs that they inflict on the host. This cost is overridden by direct benefits only if Ar/Ao is high (see also Lo´pez-Sepulcre & Kokko 2002). As the parameterization shows, Ar/Ao should reach a level that is impossible to attain with Ao ¼ 0:913. In particular, conspecific brood parasitism is not favoured at all between the closest
¨ YSA ¨ : RELATEDNESS AND BROOD PARASITISM PO
Figure 1. The empirically estimated threshold acceptance ratio, Ar/Ao, of accepting kin versus nonkin eggs in relation to the degree of hosteparasite relatedness (solid line) and the empirically estimated maximum value of Ar/Ao (dashed horizontal line), assuming perfect kin recognition in a common goldeneye population. The empirically estimated parameter values used in the example are given in the text (see Data). Relatedness promotes conspecific brood parasitism only if Ar/Ao exceeds the threshold. In the area to the left of the left-hand vertical dashed line, the threshold is unlikely to be exceeded, because hosteparasite relatedness is too low for the host to benefit from accepting eggs; i.e. equation (1) is not fulfilled. In the present common goldeneye population, kinship promotes brood parasitism only if relatedness, r, is in the area between the vertical dashed lines.
relatives (r ¼ 0:5), i.e. between mother and daughter or between full sisters. DISCUSSION
Outcome of the Empirically Parameterized Model I parameterized the biologically realistic model by Lo´pez-Sepulcre & Kokko (2002) with field data for the common goldeneye to assess the influence of relatedness and kin selection on explaining conspecific brood parasitism in the species. The parameterized model revealed that relatedness and kin selection are unlikely explanations of brood parasitism in the species, at least in the present population. In particular, parasitism was not favoured between closest relatives such as mother, daughter and sisters. As the model by Lo´pez-Sepulcre & Kokko (2002) elegantly demonstrated, the detection of brood parasitism per se and the accuracy of the kin recognition system are crucial to the conclusion whether relatedness and kin selection can promote the evolution of conspecific brood parasitism. My empirically estimated parameter values revealed that these traits cannot be particularly sophisticated in the common goldeneye. The outcome of the empirically based model exercise is in line with the predictions of the original model. Perhaps the most interesting finding of this study was that conspecific brood parasitism was not favoured between mothers and daughters and between sisters. If kin recognition in general exists in the species, one would especially expect that a daughter could recognize her mother, and sisters from the same clutch could recognize each other. The mother nearly always deserts the brood
before the young are in complete juvenile plumage (Po¨ysa¨ 1992; Po¨ysa¨ et al. 1997a), and mothers migrate to the wintering grounds several weeks earlier than daughters (H. Po¨ysa¨, unpublished data), so it is less likely that a mother could recognize her daughters, at least not by plumage. Recognition between less closely related kin (e.g. cousins) at the moment of egg laying seems unlikely, because they may not even have met before. This biological evidence and the outcome of the model exercise together strongly suggest that relatedness and kin selection are unlikely explanations of conspecific brood parasitism in the common goldeneye. My findings differ from recent observations and conclusions by Andersson & A˚hlund (2000) in another population of the same species. These authors found that host and primary parasite were more closely related than females in randomly drawn pairs and suggested that returning young females parasitize their nestmates (mothers or sisters) more often than expected by chance. Andersson & A˚hlund (2000) further concluded that genetic relatedness and kin discrimination, achieved by recognition of birth nestmates, influence conspecific brood parasitism in the species. Unfortunately, although Andersson & A˚hlund (2000) found that birth nestmates were observed together in the study lake more often than expected by chance, they did not present data on kin recognition, let alone data on kin recognition between hosts and parasites at the moment of egg laying. So, crucial information was lacking in their study, although that information is very hard to get in the field. In addition, although Andersson & A˚hlund (2000) considered philopatric nest choice in their calculations, they did not take into account that common goldeneye females in general, and experienced females in particular, prefer safe nest sites (Dow & Fredga 1983, 1985; Po¨ysa¨ et al. 2001b) and that parasites, too, preferentially lay in safe nests (Po¨ysa¨ 1999). The latter finding has recently been confirmed in an experiment with dummy nests controlling for hosteparasite relatedness (Po¨ysa¨ 2003). These traits, in addition to philopatric nest choice and spatial kin structure of breeding common goldeneye populations (e.g. daughters nest close to their mothers; Po¨ysa¨ et al. 1997b; Ruusila et al. 2001), should increase the probability that related hosts and parasites, independently and without individual recognition, lay in the same nests. Of course, differences between populations may be real, and further empirical research is needed to recognize the factors explaining the differences. Among birds, conspecific brood parasitism is particularly common in precocial species, especially among Anatidae (Eadie et al. 1988; Rohwer & Freeman 1989; Sayler 1992; Yom-Tov 2001). In addition to the common goldeneye (Andersson & A˚hlund 2000), the degree of relatedness between hosts and parasites has been studied in two other precocial ducks. Semel & Sherman (2001) found in wood ducks, Aix sponsa, that parasitic females actively avoided parasitizing close relatives, and, based on unpublished data, Lyon & Eadie (2000) mentioned that no evidence of relatedness between hosts and parasites has been found in Barrow’s goldeneyes. In moorhens, Gallinula chloropus, McRae & Burke (1996) found a high
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degree of relatedness between hosts and parasites, but that was explained by female philopatry, not by preferential laying in relatives’ nests. Hence, diverging results of the degree of hosteparasite relatedness have been reported, and there seems to be no general support for the hypothesis that relatedness and kin selection are important in explaining conspecific brood parasitism. Thus, in addition to direct measures of hosteparasite relatedness, more research of behavioural mechanisms involved in parasitic laying is needed before we can get a deeper understanding of this reproductive tactic, which occurs in a wide variety of taxa.
Adding Biological Realism Because the three components of the costs of parasitism were not strongly dependent on clutch or brood size, I used the mean value for each to estimate p(C) in the model exercise. Considering that the mean clutch size of the parasitized nests used to estimate the costs was greater than that used in the model example, one might suggest that I have overestimated the costs of parasitism. However, the use of perfect kin recognition in the model, which probably overestimates the kin recognition capacity of common goldeneye females, certainly compensated for this possible bias. Furthermore, there are two additional sources of cost of parasitism in common goldeneyes that I did not include when parameterizing p(C). First, parasitic egg laying occurs also after incubation has started (e.g. Eriksson & Andersson 1982; Eadie et al. 1995). Because parasitic eggs laid during incubation do not produce hatched ducklings, p(Cp) will be zero (this will cause only an indirect fitness cost to the host, because parasitic egg laying during incubation does not affect hatching success of host eggs: H. Po¨ysa¨, unpublished data). This cost of parasitism is particularly relevant in the context of the kin selection hypothesis. The key assumptions of the kin selection hypothesis are kin recognition and resistance to unrelated, but acceptance of related, parasites by the host (Andersson & A˚hlund 2000; Andersson 2001). In reality, incubation is the only phase of nesting when perfect kin recognition might operate and the host could accept or reject the parasite based on relatedness. However, accepting eggs from a related parasite during incubation does not make evolutionary sense, because those eggs would be wasted in the host’s nest. The second cost is caused by parasitized nests that have been deserted, which also frequently occurs in goldeneyes (e.g. Eriksson & Andersson 1982; Eadie & Fryxell 1992; Eadie et al. 1995). In the case of deserted clutches, both p(Cp) and p(Ch) will be zero, causing considerable direct and indirect fitness costs to both the host and parasite. Neither of these costs, i.e. loss of eggs laid during incubation and clutch desertion, depends on clutch size. Both of the additional costs explained above occur in the common goldeneye population studied here (H. Po¨ysa¨, unpublished data), and inclusion of them in the model exercise would have meant that kinship does not promote brood parasitism. To demonstrate this, I also included those nests in which parasitic eggs were laid after
incubation had started (five additional nests that proceeded to hatching and nest exodus), and recalculated the mean values for p(H) and p(L) and, finally, estimated a new pðCh þ Cp Þ for the parasitized nests. The new values are pðHÞ ¼ 0:896, pðLÞ ¼ 0:985 and pðCh þ Cp Þ ¼ 0:603. I repeated the model exercise by using the new estimate for pðCh þ Cp Þ and keeping all the other parameter values the same as in Fig. 1. It turned out that relatedness does not promote brood parasitism in the present common goldeneye population, because equation (1) is fulfilled only if r > 0:369 and the empirically estimated maximum Ar/Ao (i.e. 1.095) falls below the new threshold acceptance ratio for all r > 0:369; the empirically estimated maximum Ar/Ao crosses the new threshold acceptance ratio curve at r ¼ 0:235. Inclusion of parasitized nests that were deserted (N ¼ 19) would drastically decrease the overall value of pðCh þ Cp Þ, because in the deserted nests, pðCh þ Cp Þ is zero (see above), increasing considerably the cost of parasitism and, hence, making it less and less likely that relatedness could promote brood parasitism. I conclude that the empirically based model exercise of the present study is conservative enough in rejecting relatedness and kin selection as explanations of brood parasitism in the species. Acknowledgments I thank H. Kokko, V. Ruusila, J. Sorjonen and three anonymous referees for useful comments on the manuscript. References A˚hlund, M. & Andersson, M. 2001. Female ducks can double their reproduction. Nature, 414, 600e601. Andersson, M. 1984. Brood parasitism within species. In: Producers and Scroungers: Strategies of Exploitation and Parasitism (Ed. by C. J. Barnard), pp. 195e228. London: Croom Helm. Andersson, M. 2001. Relatedness and the evolution of conspecific brood parasitism. American Naturalist, 158, 599e614. Andersson, M. & A˚hlund, M. 2000. Hosteparasite relatedness shown by protein fingerprinting in a brood parasitic bird. Proceedings of the National Academy of Sciences, U.S.A., 97, 13188e13193. Andersson, M. & A˚hlund, M. 2001. Protein fingerprinting: a new technique reveals extensive conspecific brood parasitism. Ecology, 82, 1433e1442. Andersson, M. & Eriksson, M. O. G. 1982. Nest parasitism in goldeneyes Bucephala clangula: some evolutionary aspects. American Naturalist, 120, 1e16. Broom, M. & Ruxton, G. D. 2002. A game theoretical approach to conspecific brood parasitism. Behavioral Ecology, 13, 321e327. Bulmer, M. G. 1984. Risk avoidance and nesting strategies. Journal of Theoretical Biology, 106, 529e535. Dow, H. & Fredga, S. 1983. Breeding and natal dispersal of the goldeneye, Bucephala clangula. Journal of Animal Ecology, 52, 681e695. Dow, H. & Fredga, S. 1985. Selection of nest sites by a hole-nesting duck, the goldeneye Bucephala clangula. Ibis, 127, 16e30. Eadie, J. M. 1989. Alternative reproductive tactics in a precocial bird: the ecology and evolution of brood parasitism in goldeneyes. Ph.D. thesis, University of British Columbia.
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Eadie, J. M. & Fryxell, J. M. 1992. Density dependence, frequency dependence, and alternative nesting strategies in goldeneyes. American Naturalist, 140, 621e641. Eadie, J. M., Kehoe, F. P. & Nudds, T. D. 1988. Pre-hatch and posthatch brood amalgamation in North American Anatidae: a review. Canadian Journal of Zoology, 66, 1709e1721. Eadie, J. M., Mallory, M. L. & Lumsden, H. G. 1995. Common goldeneye Bucephala clangula. In: The Birds of North America, No. 170 (Ed. by A. Poole & E. Gill), pp. 1e32. Philadelphia: The Academy of Natural Sciences. Eriksson, M. O. G. 1978. Lake selection by goldeneye ducklings in relation to the abundance of food. Wildfowl, 29, 81e85. Eriksson, M. O. G. 1979. Aspects of the breeding biology of the goldeneye Bucephala clangula. Holarctic Ecology, 2, 186e194. Eriksson, M. O. G. & Andersson, M. 1982. Nest parasitism and hatching success in a population of goldeneyes Bucephala clangula. Bird Study, 29, 49e54. Lo´pez-Sepulcre, A. & Kokko, H. 2002. The role of kin recognition in the evolution of conspecific brood parasitism. Animal Behaviour, 64, 215e222. Lyon, B. E. & Eadie, J. M. 2000. Family matters: kin selection and the evolution of conspecific brood parasitism. Proceedings of the National Academy of Sciences, U.S.A., 97, 12942e12944. McRae, S. B. & Burke, T. 1996. Intraspecific brood parasitism in the moorhen: parentage and parasiteehost relationships determined by DNA fingerprinting. Behavioral Ecology and Sociobiology, 38, 115e129. Milonoff, M. & Paananen, P. 1993. Egg formation, brood survival, and cost of reproduction as clutch-size-determining factors in common goldeneyes. Auk, 110, 943e946. ¨ ysa¨, H. & Virtanen, J. 1995. Brood-size dependent Milonoff, M., Po offspring mortality in common goldeneyes reconsidered: fact or artifact? American Naturalist, 146, 967e974. ¨ ysa¨, H. & Runko, P. 1998. Factors affecting clutch Milonoff, M., Po size and duckling survival in the common goldeneye Bucephala clangula. Wildlife Biology, 4, 73e80. Petrie, M. & Møller, A. P. 1991. Laying eggs in others’ nests: intraspecific brood parasitism in birds. Trends in Ecology and Evolution, 6, 315e320. ¨ ysa¨, H. 1992. Variation in parental care of common goldeneye Po (Bucephala clangula) females. Behaviour, 123, 247e260. ¨ ysa¨, H. 1999. Conspecific nest parasitism is associated with Po inequality in nest predation risk in the common goldeneye (Bucephala clangula). Behavioral Ecology, 10, 533e540. ¨ ysa¨, H. 2003. Parasitic common goldeneye (Bucephala clangula) Po females lay preferentially in safe neighbourhoods. Behavioral Ecology and Sociobiology, 54, 30e35. ¨ ysa¨, H. & Milonoff, M. 1999. Processes underlying parental care Po decisions and cre`ching behaviour: clarification of hypotheses. Annales Zoologici Fennici, 36, 125e128. ¨ ysa¨, H. & Po ¨ ysa¨, S. 2002. Nest-site limitation and density Po dependence of reproductive output in the common goldeneye Bucephala clangula: implications for the management of cavitynesting birds. Journal of Applied Ecology, 39, 502e510. ¨ ysa¨, H. & Virtanen, J. 1994. Habitat selection and survival of Po common goldeneye (Bucephala clangula) broods: preliminary results. Hydrobiologia, 279/280, 289e296.
¨ ysa¨, H., Virtanen, J. & Milonoff, M. 1997a. Common goldeneyes Po adjust maternal effort in relation to prior brood success and not current brood size. Behavioral Ecology and Sociobiology, 40, 101e106. ¨ ysa¨, H., Runko, P. & Ruusila, V. 1997b. Natal philopatry and the Po local resource competition hypothesis: data from the common goldeneye. Journal of Avian Biology, 28, 63e67. ¨ ysa¨, H., Milonoff, M., Ruusila, V. & Virtanen, J. 1999. Nest-site Po selection in relation to habitat edge: experiments in the common goldeneye. Journal of Avian Biology, 30, 79e84. ¨ ysa¨, H., Runko, P., Ruusila, V. & Milonoff, M. 2001a. Po Identification of parasitized nests by using egg morphology in the common goldeneye: an alternative to blood sampling. Journal of Avian Biology, 32, 79e82. ¨ ysa¨, H., Ruusila, V., Milonoff, M. & Virtanen, J. 2001b. Ability to Po assess nest predation risk in secondary hole-nesting birds: an experimental study. Oecologia, 126, 201e207. Rohwer, F. C. 1988. Inter- and intraspecific relationships between egg size and clutch size in waterfowl. Auk, 105, 161e176. Rohwer, F. C. & Freeman, S. 1989. The distribution of conspecific nest parasitism in birds. Canadian Journal of Zoology, 67, 239e253. Rubenstein, D. I. 1982. Risk, uncertainty and evolutionary strategies. In: Current Problems in Sociobiology (Ed. by King’s College Sociobiology Group), pp. 91e111. Cambridge: Cambridge University Press. ¨ ysa¨, H. & Runko, P. 2000. Characteristics of maternal Ruusila, V., Po family lineages in a common goldeneye Bucephala clangula breeding population. Ornis Fennica, 77, 77e82. ¨ ysa¨, H. & Runko, P. 2001. Costs and benefits of Ruusila, V., Po female-biased natal philopatry in the common goldeneye. Behavioral Ecology, 12, 686e690. Savard, J.-P. L., Smith, G. E. J. & Smith, J. N. M. 1991. Duckling mortality in Barrow’s goldeneye and bufflehead broods. Auk, 108, 568e577. Sayler, R. D. 1992. Ecology and evolution of brood parasitism in waterfowl. In: Ecology and Management of Breeding Waterfowl (Ed. by B. D. J. Batt, A. D. Afton, M. G. Anderson, C. D. Ankney, D. H. Johnson, J. A. Kadlec & G. L. Krapu), pp. 290e322. Minneapolis: University of Minnesota Press. Semel, B. & Sherman, P. W. 2001. Intraspecific parasitism and nest-site competition in wood ducks. Animal Behaviour, 61, 787e803. Sire´n, M. 1952. Studies on the breeding biology of the goldeneye, Bucephala clangula (in Swedish with English summary). Papers on Game Research, 8, 101e111. Sire´n, M. 1956. Telka¨n, Bucephala clangula (L.), lisa¨a¨ntymisbiologiaa (in Finnish). Licentiate thesis, University of Helsinki. Wayland, M. & McNicol, D. K. 1994. Movements and survival of common goldeneye broods near Sudbury, Ontario, Canada. Canadian Journal of Zoology, 72, 1252e1259. Yom-Tov, Y. 2001. An updated list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis, 143, 133e143. Zink, A. G. 2000. The evolution of intraspecific brood parasitism in birds and insects. American Naturalist, 155, 395e405.
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Relatedness and the evolution of conspecific brood parasitism: parameterizing a model with data for a precocial species ¨ YS A ¨ H AN N U P O
Finnish Game and Fisheries Research Institute, Joensuu Game and Fisheries Research (Received 25 November 2002; initial acceptance 7 February 2003; final acceptance 4 August 2003; MS. number: 7547R)
Conspecific brood parasitism (CBP) is a common reproductive tactic in several animal taxa, especially in precocial birds. It has been suggested that hosteparasite relatedness can facilitate the evolution of CBP. A recent model showed that the existence and accuracy of the kin recognition system is crucial for this to occur. I used field data to parameterize the model for the common goldeneye, Bucephala clangula, a precocial species in which CBP frequently occurs and in which a recent finding of nonrandom hosteparasite relatedness has been interpreted to support the idea that relatedness and kin selection influence CBP. It turned out that possibilities to detect brood parasitism and accurately discriminate between kin and nonkin parasites are negligible in the species. The empirically parameterized model exercise revealed that relatedness and kin selection are unlikely explanations of CBP in the species. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Conspecific brood parasitism is an alternative reproductive tactic in which a female lays eggs in the nest of a conspecific female that takes care of incubation and the young. Several hypotheses have been put forward to explain the evolution of this reproductive tactic (Andersson 1984; Eadie et al. 1988; Petrie & Møller 1991; Sayler 1992). The subject in general has received considerable theoretical attention (e.g. Rubenstein 1982; Andersson 1984, 2001; Bulmer 1984; Eadie & Fryxell 1992; Zink 2000; Broom & Ruxton 2002; Lo´pez-Sepulcre & Kokko 2002). In particular, the role of kin selection in the evolution of conspecific brood parasitism has recently been in focus (Zink 2000; Andersson 2001; Lo´pez-Sepulcre & Kokko 2002). The models by Zink (2000), Andersson (2001) and Lo´pez-Sepulcre & Kokko (2002) differ in several important aspects and assumptions (see also Lyon & Eadie 2000) and, because of that, the models also reach diverging conclusions about the influence of kin selection on the evolution of conspecific brood parasitism. In brief, although one of the main findings of Zink (2000) was that relatedness should not promote the evolution of conspecific brood parasitism, Andersson’s (2001) model suggested that it can. One of the basic differences between Zink (2000) and Andersson (2001) was that their models assumed different levels of cost from parasitism. In Zink’s model, the direct cost for a parasitized host was assumed Correspondence: H. Po¨ysa¨, Finnish Game and Fisheries Research Institute, Joensuu Game and Fisheries Research, Kauppakatu 18-20, FIN-80100 Joensuu, Finland (email: hannu.poysa@rktl.fi). 0003e3472/03/$30.00/0
to be large (i.e. a host clutch size is reduced by the exact number of parasitic eggs laid in the nest), but in Andersson’s model, the direct costs were assumed to be small or moderate. In general, if direct costs of parasitism are large, hosteparasite relatedness will not make parasitism advantageous and, hence, it is better to parasitize an unrelated host (see also Andersson 2001, page 607). While taking into account the different approaches of Zink (2000) and Andersson (2001) concerning the costs of parasitism, Lo´pez-Sepulcre & Kokko (2002) focused on the role of kin recognition that was assumed to be perfect in Andersson’s (2001) model. Their model revealed that the existence and accuracy of a kin recognition system is crucial to determine whether parasitism should be directed towards relatives or nonrelatives. If parasitism is costly to the host, and the host cannot accurately discriminate between related and unrelated parasites, kinship will not promote the evolution of conspecific brood parasitism. The above discussion demonstrates how crucial it is to build models on biologically realistic assumptions and parameter values to understand the influence of relatedness and kin selection on the evolution of conspecific brood parasitism. Lo´pez-Sepulcre & Kokko’s (2002) model made a valuable contribution to the subject, because it was based on biologically realistic assumptions and identified the crucial importance of the accuracy of kin recognition, a parameter that has not been empirically measured so far. The other critical model parameter that has been difficult to estimate with field data is the cost of parasitism (but see Eadie & Fryxell 1992). We need
673 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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empirical studies to get biologically realistic estimates of the critical model parameters for different species and reproductive strategies. In this paper, I use field data to parameterize Lo´pezSepulcre & Kokko’s (2002) model for the common goldeneye, Bucephala clangula, a precocial hole-nesting species in which conspecific brood parasitism occurs frequently and has been intensively studied (review in Eadie et al. 1995; see also Po¨ysa¨ 1999; Andersson & ˚ hlund 2000). By doing that, I assessed the plausibility of A relatedness and kin selection in explaining brood parasitism in the species. Andersson & A˚hlund (2000) found in a Swedish common goldeneye population that hosts and the primary parasite were more closely related than females in random pairs. They suggested that relatedness and kin discrimination, achieved by recognition of birth nestmates, influence conspecific brood parasitism in the species. In the present study, I focused on the kin recognition system, especially on the possibilities of hosts detecting parasitism in the first place. I also estimated the other model parameters, including the costs of parasitism, by using long-term field data from a Finnish common goldeneye population (Po¨ysa¨ 1999).
THE MODEL Details of the derivation of the full model can be found in Lo´pez-Sepulcre & Kokko (2002). The model parameters are as follows (see Table 1, Lo´pez-Sepulcre & Kokko 2002): Co Z number of eggs laid by a nonparasitic female in a nest without parasitism; Cp Z number of eggs laid by a parasitic female in the host’s nest; Ch Z number of eggs laid by a nonparasitic female when parasitized; p(C) Z proportion of eggs that give young surviving to fledging age; r Z coefficient of genetic relatedness between host and parasite; Ao Z probability of accepting eggs laid by a nonrelative (0%Ao %1); Ar Z probability of accepting eggs laid by a relative (0 % Ar % 1) in the host’s nest. I focused on a submodel addressing a case in which kin recognition is not necessarily perfect and parasitism is costly. In such a case, relatedness will favour brood parasitism if the following equations are satisfied simultaneously (equations 9 and 12 in Lo´pez-Sepulcre & Kokko 2002): r>
Co pðCo ÞCh pðCh þCp Þ Cp pðCh þCp Þ
ð1Þ
and Ar =Ao >
Cp pðCh þCp Þ Cp pðCh þCp Þþr½Ch pðCh þCp ÞCo pðCo Þ
ð2Þ
If there are fitness costs from parasitism, equation (1) specifies the degree of relatedness between host and parasite that must be exceeded before accepting parasitic eggs from a kin is advantageous. Equation (2) in turn specifies a threshold value for the accuracy of kin recognition, Ar/Ao, so that relatedness could promote conspecific brood parasitism; this happens only if related eggs are sufficiently more likely to be accepted than nonkin eggs, i.e. Ar/Ao exceeds the threshold (Lo´pez-
Sepulcre & Kokko 2002). These two quantities, r and Ar/Ao, are under consideration when exploring the parameterized model in the present study. DATA All data are from a common goldeneye population (Intsila¨) in which conspecific brood parasitism and other aspects of the breeding ecology of the species have been ¨ ysa¨ studied intensively since 1992 (Milonoff et al. 1995; Po ¨ ysa¨ et al. 1997a, 1999, 2001b; Po¨ysa¨ 1999; Po¨ysa¨ & Po 2002); data are from 1992e2002 if not otherwise specified. Especially Po¨ysa¨ (1999) and Po¨ysa¨ & Po¨ysa¨ (2002) are referred to for description of the study area and for general methods used in the gathering of nesting data. Most common goldeneye females breed in nestboxes that are available in excess in the area. Most data are from individually known females (ringed and wing tagged; licence from the Finnish Museum of Natural History, University of Helsinki); if data from more than 1 year were available for a given female, I included only one, randomly selected year in the calculations for that female. In the following I explain the data for each of the parameters in the model, except r and Ar, whose possible values are under consideration when exploring the parameterized model.
Clutch Size: Co, Cp and Ch I included all nesting attempts that proceeded to hatching and nest exodus and for which I succeeded in measuring all the eggs; deserted and predated (partially or totally) clutches were not included. I also estimated the start of incubation in each nest as exactly as possible and excluded those nests for which I knew that parasitic eggs were laid after incubation had started. Because in these nests the parasitic eggs would not hatch at all (i.e. incubation time too short; hatched ducklings leave the nest 24e36 h after hatching, Eadie et al. 1995), the cost of parasitism to the host is exceptionally high, although the host will face only an indirect fitness cost if the eggs are laid by a relative. Exclusion of these nests only makes my analysis more conservative. Width and length of all eggs in the clutches were measured, and weights of the eggs were estimated using the formulae developed by Rohwer (1988) for waterfowl. Based on the within-clutch variation (Euclidean distance) of these three egg characteristics, I identified parasitized and nonparasitized nests with a method developed by and explained in Eadie (1989) and later explained, tested and used in Po¨ysa¨ (1999) and Po¨ysa¨ et al. (2001a). If egg size is strongly heritable, the method used to identify parasitized nests might fail to recognize nests parasitized by relatives. Hence, in the present data, some of the clutches that were identified as nonparasitized might in fact have been parasitized by relatives. This seems unlikely, however. First, mean size of clutches that were identified as nonparasitized was 7.0, but that of clutches identified as parasitized was 11.7. If some of the nonparasitized clutches were in fact parasitized, it would mean that host clutch size was, on
¨ YSA ¨ : RELATEDNESS AND BROOD PARASITISM PO
average, about five eggs, an exceptionally small clutch for common goldeneyes (e.g. Eadie et al. 1995). Second, Andersson & A˚hlund (2001) identified parasitized and nonparasitized nests based on protein fingerprinting, a technique that also identifies nests parasitized by close relatives. In their data (Table 4), the mean size of nonparasitized clutches was 7.8, i.e. very close to that in the present study, and the mean number of host eggs in parasitized clutches was 7.9. Hence, I conclude that the method used to identify parasitized and nonparasitized clutches did not bias the data. Mean G SD size of nonparasitized clutches was 7:0 G 1:8 (N Z 15) and of parasitized clutches 11:7 G 2:9 (N Z 31). There is no evidence in the common goldeneye that hosts would decrease their own clutch size in response to parasitism (Sayler 1992; see also Andersson 2001, page 610), so I assumed that Co ZCh Z7, a typical clutch size of nonparasitized nests in the species (Eadie et al. 1995). A direct measure for Cp is not available from the present population. Based on data in Table 4 (H, hatched clutches that were parasitized) of Andersson & A˚hlund (2001), I calculated that the mean number of parasitic eggs per parasitizing female was 2.2 (N ¼ 8); therefore I assumed that Cp ¼ 2:2. In reality, some nests may be parasitized by more than one female (i.e. mean size of parasitized clutches was 11.7) but the costs of parasitism are not strongly dependent on clutch size.
From Eggs to Fledged Young: p(C ) In the case of the common goldeneye, the proportion of eggs that give young surviving to fledging age is a product of three components: the proportion of eggs that hatch ( p(H)), the proportion of hatched ducklings that leave the nest ( p(L)) and the proportion of ducklings leaving the nest that survive until fledging ( p(F)). Because common goldeneye broods frequently change lake soon after nest exodus (Eriksson 1978, 1979; Po¨ysa¨ & Virtanen 1994; Wayland & McNicol 1994), it was impossible to get data for duckling survival for all the broods that left the nest; therefore, sample size was smaller for the brood phase than for the nest phase. Brood mortality in goldeneyes is highest during the first week after nest exodus (Savard et al. 1991; Milonoff et al. 1995; Po¨ysa¨ et al. 1997a), and mortality rate during the first week is a good predictor of mortality rate after the first week until the age of 40 days (Po¨ysa¨ et al. 1997a; see also Po¨ysa¨ & Milonoff 1999). Also, the duration of maternal care depends on prior brood survival in the common goldeneye, and many females desert the brood within the first 2 weeks after nest exodus ¨ ysa¨ et al. 1997a; Po¨ysa¨ & Milonoff 1999). (Po¨ysa¨ 1992; Po Therefore, to get as large and unbiased a data set as possible, I estimated the proportion of fledged young by using broods that I was able to follow individually until the end of the first week after nest exodus. The proportions explained above showed varying responses to clutch or brood size: p(H) was not significantly associated with clutch size (Spearman rank correlation: rS ¼ 0:198, N ¼ 46, NS; range of clutch size 4e16), p(L) decreased with increasing number of hatched
ducklings (rS ¼ 0:382, N ¼ 46, P!0:01; range of the number of hatched ducklings 4e16), and there was no association between p(F) and brood size (rS ¼ 0:008, N ¼ 29, NS; range of brood size 3e16). Andersson & Eriksson (1982) showed that almost all eggs hatched, regardless of clutch size, in successful common goldeneye nests. They concluded that addition of parasitic eggs during the host’s laying period should not markedly reduce hatching success, i.e. p(H) should be independent of clutch size. I am not aware of common goldeneye studies in which the relation between p(L) and the number of hatched ducklings has been examined. However, the negative relation between p(L) and the number of hatched ducklings is biologically realistic. At nest departure, the female is calling for the ducklings outside the nest cavity and the ducklings jump one at a time out from the nest (Eadie et al. 1995). Hence, because the strength-demanding nest departure depends on each duckling’s own condition, and because it may take longer for a larger brood to leave the nest (in Sire´n’s 1952 data of five broods with 4, 5, 6, 9 and 9 ducklings, the departure of the young took 40, 105, 95, 86 and 150 s, respectively), making the nest departure exposed to disturbance for a longer period, one or more of the last ducklings of a large brood may not get out from the nest cavity. Sire´n (1956) described cases in which the female abandoned live ducklings in the nestbox and led away the ducklings that had jumped out. As to the lack of association between p(F) and brood size, observational and experimental results from common goldeneye populations have consistently shown that p(F) is independent of brood size (Milonoff & Paananen 1993; Milonoff et al. 1995, 1998; Po¨ysa¨ et al. 1997a). Andersson & Eriksson (1982) reported that p(F) was a negative function of brood size (but see Milonoff et al. 1995), but Eadie & Fryxell (1992) reported that p(F) was a positive function of brood size in the closely related Barrow’s goldeneye, B. islandica. In sum, the present data did not show strong dependence of p(H), p(L) and p(F) on clutch or brood size, so I decided to use mean values of the proportions, as follows: nonparasitized nests: pðHÞ ¼ 0:961, N ¼ 15; pðLÞ ¼ 1:0, N ¼ 15; pðFÞ ¼ 0:700, N ¼ 12; parasitized nests: pðHÞ ¼ 0:928, N ¼ 31; pðLÞ ¼ 0:988, N ¼ 31; pðFÞ ¼ 0:683, N ¼ 17. These proportions are independent (p(H) versus p(L): Spearman rank correction: rS ¼ 0:064, N ¼ 46, NS; p(H) versus p(F): rS ¼ 0:131, N ¼ 29, NS; p(L) versus p(F): rS ¼ 0:095, N ¼ 29, NS). Therefore, the proportion of eggs that give young surviving to fledging age, p(C), can be calculated as the product of the three proportions, resulting in the following parameter estimates: nonparasitized nests: pðCo Þ ¼ 0:673; parasitized nests: pðCh þ Cp Þ ¼ 0:626.
Accuracy of Kin Recognition: Ar/Ao Common goldeneye females do not defend the nest during the egg-laying period (Eadie et al. 1995). Recognition and rejection or removal of parasitic eggs is also unlikely in common goldeneyes. For example, Andersson &
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Eriksson (1982) experimentally added several parasitic eggs to the nests of common goldeneyes and found no evidence of egg eviction from the nests. They also suggested that identification and eviction of eggs laid by other females may usually be impossible because of the deep and dark nest cavity. Similarly, Milonoff & Paananen (1993) experimentally added eggs from other females in some common goldeneye nests and found that hatching success in these nests did not decrease, implying indirectly that the recipient females did not discriminate against the strange eggs. Hence, the only biologically realistic possibility for the host to detect and reject a nonkin potential parasite is when the host herself visits the nest for egg laying (i.e. the host could prevent the parasite entering the nest). In general, the intervals between eggs are about 1.3e2 days (Eadie et al. 1995). Similarly, Andersson & ˚ hlund’s (2000) video recordings revealed that hosts A during the laying period usually visit the nest only every other day. As Lo´pez-Sepulcre & Kokko (2002, page 218) noted, the value of Ar/Ao summarizes both the effects of kin recognition (i.e. whether Ar > Ao ) and the detection of brood parasitism per se (the absolute value of Ao). Although I do not have data to estimate Ar and Ao directly and separately, I was able to estimate the probability that a host could detect and reject parasitic laying as follows. Related to an ongoing field experiment of conspecific brood parasitism in the common goldeneye (H. Po¨ysa¨, unpublished data), I frequently visited the nestboxes during the laying phase in 1999e2002. During each visit, I recorded whether a female was in the nestbox or whether a female left the nestbox when I approached it. I included only nests that proceeded to incubation (i.e. I was sure that a nest had a host), and there were 68 such nests in all. For each nest, I included only visits after the first egg had been laid and before the incubation had started. Mean G SD number of visits per nest was 5:6G2:9 and the mean length of the period over which the visits were distributed was 8:3G4:1 days per nest. In all, I made 379 such visits to the nests between 0700 and 2100 hours, and I saw a female in the nestbox or the female left the nestbox when I approached it in 33 of the 379 cases. Most of the visits were made between 1100 and 1600 hours (53.8%) and fewer between 0700 and 1100 hours (20.8%) and 1600 and 2100 hours (25.3%). However, the proportion of the visits when a female was in the nestbox did not differ between the three periods (chisquare test: c22 ¼ 3:48, NS). Furthermore, on 22 visits, I recognized a newly laid egg (one of the eggs was much warmer than the other eggs in the clutch; I interpreted that the egg had been laid within the last 2 h before my visit); 10 of these eggs were laid between 0700 and 1100 hours, 10 between 1100 and 1600 hours and two between 1600 and 2100 hours, i.e. egg laying occurred throughout the day. I conclude that my visits to the nestboxes provide a biologically sound way to measure the probability of a host being in the nestbox if a parasitic female tries to enter it for egg laying. These figures can be used to estimate the probability that a host female in general can detect and reject parasitic laying in the common
goldeneye (33=379 ¼ 0:087; this figure is probably an overestimate, because some of the females I saw in the nestboxes may have been laying parasites). The estimated probability is low but not exceptional, considering the biological facts we know about the laying behaviour of common goldeneye females. I used this probability to approximate Ao as follows: Ao ¼ 1 0:087 ¼ 0:913. Even though this measure does not make a difference between nonrelative and relative eggs, it gives the approximate minimum probability for accepting a nonrelative egg, i.e. the ‘true’ value of Ao should be between 0.913 and 1. This is because in common goldeneyes we can assume that a parasitic egg is always accepted if parasitism is not detected (i.e. the host is not in the nest). Using the minimum value of 0.913 for Ao and assuming perfect kin recognition make the model exercise most conservative. Finally, as in the original model (Lo´pez-Sepulcre & Kokko 2002, page 220), I assume that parasites have the choice of finding unrelated females’ nests. This is a realistic assumption in common goldeneyes, because, even though nest site fidelity and female natal philopatry are high in the species (Dow & Fredga 1983; Po¨ysa¨ et al. 1997b; Ruusila et al. 2001), most of the nesting females do not have relatives breeding at the same time in the area (Ruusila et al. 2000). Furthermore, within the same season, a given parasitic female may lay in nests several kilometres apart (Andersson & A˚hlund 2000; A˚hlund & Andersson 2001; Po¨ysa¨ 2003). This evidence means that, in general, the likelihood of being parasitized by a relative should not be higher than that of being parasitized by a nonrelative.
RESULTS If hosts rarely detect brood parasitism, Ao is near 1, and Ar/Ao cannot be high because 0 % Ar % 1 (Lo´pez-Sepulcre & Kokko 2002). In the present common goldeneye population, Ao was estimated to be 0.913. Hence, if we assume perfect kin recognition (i.e. Ar ¼ 1), Ar/Ao has a maximum value of 1.095. Perfect kin recognition is probably unrealistic in common goldeneyes, but I focus on it to make my conclusions about the role of the kin selection hypothesis in explaining conspecific brood parasitism in the species as conservative as possible. The empirically estimated maximum value of Ar/Ao means that, in the present common goldeneye population, close relatedness does not enhance conspecific brood parasitism. Even assuming perfect kin recognition, the range of relatedness, r, where both equations (1) and (2) are fulfilled is narrow (0:239 ! r ! 0:364; Fig. 1, area between the vertical dashed lines). At small values of r, brood parasitism between kin is not favoured because hosts are not selected to accept costly parasitism from too remotely related parasites. At large values of r, parasites are not selected to target related hosts, because they suffer from indirect costs that they inflict on the host. This cost is overridden by direct benefits only if Ar/Ao is high (see also Lo´pez-Sepulcre & Kokko 2002). As the parameterization shows, Ar/Ao should reach a level that is impossible to attain with Ao ¼ 0:913. In particular, conspecific brood parasitism is not favoured at all between the closest
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Figure 1. The empirically estimated threshold acceptance ratio, Ar/Ao, of accepting kin versus nonkin eggs in relation to the degree of hosteparasite relatedness (solid line) and the empirically estimated maximum value of Ar/Ao (dashed horizontal line), assuming perfect kin recognition in a common goldeneye population. The empirically estimated parameter values used in the example are given in the text (see Data). Relatedness promotes conspecific brood parasitism only if Ar/Ao exceeds the threshold. In the area to the left of the left-hand vertical dashed line, the threshold is unlikely to be exceeded, because hosteparasite relatedness is too low for the host to benefit from accepting eggs; i.e. equation (1) is not fulfilled. In the present common goldeneye population, kinship promotes brood parasitism only if relatedness, r, is in the area between the vertical dashed lines.
relatives (r ¼ 0:5), i.e. between mother and daughter or between full sisters. DISCUSSION
Outcome of the Empirically Parameterized Model I parameterized the biologically realistic model by Lo´pez-Sepulcre & Kokko (2002) with field data for the common goldeneye to assess the influence of relatedness and kin selection on explaining conspecific brood parasitism in the species. The parameterized model revealed that relatedness and kin selection are unlikely explanations of brood parasitism in the species, at least in the present population. In particular, parasitism was not favoured between closest relatives such as mother, daughter and sisters. As the model by Lo´pez-Sepulcre & Kokko (2002) elegantly demonstrated, the detection of brood parasitism per se and the accuracy of the kin recognition system are crucial to the conclusion whether relatedness and kin selection can promote the evolution of conspecific brood parasitism. My empirically estimated parameter values revealed that these traits cannot be particularly sophisticated in the common goldeneye. The outcome of the empirically based model exercise is in line with the predictions of the original model. Perhaps the most interesting finding of this study was that conspecific brood parasitism was not favoured between mothers and daughters and between sisters. If kin recognition in general exists in the species, one would especially expect that a daughter could recognize her mother, and sisters from the same clutch could recognize each other. The mother nearly always deserts the brood
before the young are in complete juvenile plumage (Po¨ysa¨ 1992; Po¨ysa¨ et al. 1997a), and mothers migrate to the wintering grounds several weeks earlier than daughters (H. Po¨ysa¨, unpublished data), so it is less likely that a mother could recognize her daughters, at least not by plumage. Recognition between less closely related kin (e.g. cousins) at the moment of egg laying seems unlikely, because they may not even have met before. This biological evidence and the outcome of the model exercise together strongly suggest that relatedness and kin selection are unlikely explanations of conspecific brood parasitism in the common goldeneye. My findings differ from recent observations and conclusions by Andersson & A˚hlund (2000) in another population of the same species. These authors found that host and primary parasite were more closely related than females in randomly drawn pairs and suggested that returning young females parasitize their nestmates (mothers or sisters) more often than expected by chance. Andersson & A˚hlund (2000) further concluded that genetic relatedness and kin discrimination, achieved by recognition of birth nestmates, influence conspecific brood parasitism in the species. Unfortunately, although Andersson & A˚hlund (2000) found that birth nestmates were observed together in the study lake more often than expected by chance, they did not present data on kin recognition, let alone data on kin recognition between hosts and parasites at the moment of egg laying. So, crucial information was lacking in their study, although that information is very hard to get in the field. In addition, although Andersson & A˚hlund (2000) considered philopatric nest choice in their calculations, they did not take into account that common goldeneye females in general, and experienced females in particular, prefer safe nest sites (Dow & Fredga 1983, 1985; Po¨ysa¨ et al. 2001b) and that parasites, too, preferentially lay in safe nests (Po¨ysa¨ 1999). The latter finding has recently been confirmed in an experiment with dummy nests controlling for hosteparasite relatedness (Po¨ysa¨ 2003). These traits, in addition to philopatric nest choice and spatial kin structure of breeding common goldeneye populations (e.g. daughters nest close to their mothers; Po¨ysa¨ et al. 1997b; Ruusila et al. 2001), should increase the probability that related hosts and parasites, independently and without individual recognition, lay in the same nests. Of course, differences between populations may be real, and further empirical research is needed to recognize the factors explaining the differences. Among birds, conspecific brood parasitism is particularly common in precocial species, especially among Anatidae (Eadie et al. 1988; Rohwer & Freeman 1989; Sayler 1992; Yom-Tov 2001). In addition to the common goldeneye (Andersson & A˚hlund 2000), the degree of relatedness between hosts and parasites has been studied in two other precocial ducks. Semel & Sherman (2001) found in wood ducks, Aix sponsa, that parasitic females actively avoided parasitizing close relatives, and, based on unpublished data, Lyon & Eadie (2000) mentioned that no evidence of relatedness between hosts and parasites has been found in Barrow’s goldeneyes. In moorhens, Gallinula chloropus, McRae & Burke (1996) found a high
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degree of relatedness between hosts and parasites, but that was explained by female philopatry, not by preferential laying in relatives’ nests. Hence, diverging results of the degree of hosteparasite relatedness have been reported, and there seems to be no general support for the hypothesis that relatedness and kin selection are important in explaining conspecific brood parasitism. Thus, in addition to direct measures of hosteparasite relatedness, more research of behavioural mechanisms involved in parasitic laying is needed before we can get a deeper understanding of this reproductive tactic, which occurs in a wide variety of taxa.
Adding Biological Realism Because the three components of the costs of parasitism were not strongly dependent on clutch or brood size, I used the mean value for each to estimate p(C) in the model exercise. Considering that the mean clutch size of the parasitized nests used to estimate the costs was greater than that used in the model example, one might suggest that I have overestimated the costs of parasitism. However, the use of perfect kin recognition in the model, which probably overestimates the kin recognition capacity of common goldeneye females, certainly compensated for this possible bias. Furthermore, there are two additional sources of cost of parasitism in common goldeneyes that I did not include when parameterizing p(C). First, parasitic egg laying occurs also after incubation has started (e.g. Eriksson & Andersson 1982; Eadie et al. 1995). Because parasitic eggs laid during incubation do not produce hatched ducklings, p(Cp) will be zero (this will cause only an indirect fitness cost to the host, because parasitic egg laying during incubation does not affect hatching success of host eggs: H. Po¨ysa¨, unpublished data). This cost of parasitism is particularly relevant in the context of the kin selection hypothesis. The key assumptions of the kin selection hypothesis are kin recognition and resistance to unrelated, but acceptance of related, parasites by the host (Andersson & A˚hlund 2000; Andersson 2001). In reality, incubation is the only phase of nesting when perfect kin recognition might operate and the host could accept or reject the parasite based on relatedness. However, accepting eggs from a related parasite during incubation does not make evolutionary sense, because those eggs would be wasted in the host’s nest. The second cost is caused by parasitized nests that have been deserted, which also frequently occurs in goldeneyes (e.g. Eriksson & Andersson 1982; Eadie & Fryxell 1992; Eadie et al. 1995). In the case of deserted clutches, both p(Cp) and p(Ch) will be zero, causing considerable direct and indirect fitness costs to both the host and parasite. Neither of these costs, i.e. loss of eggs laid during incubation and clutch desertion, depends on clutch size. Both of the additional costs explained above occur in the common goldeneye population studied here (H. Po¨ysa¨, unpublished data), and inclusion of them in the model exercise would have meant that kinship does not promote brood parasitism. To demonstrate this, I also included those nests in which parasitic eggs were laid after
incubation had started (five additional nests that proceeded to hatching and nest exodus), and recalculated the mean values for p(H) and p(L) and, finally, estimated a new pðCh þ Cp Þ for the parasitized nests. The new values are pðHÞ ¼ 0:896, pðLÞ ¼ 0:985 and pðCh þ Cp Þ ¼ 0:603. I repeated the model exercise by using the new estimate for pðCh þ Cp Þ and keeping all the other parameter values the same as in Fig. 1. It turned out that relatedness does not promote brood parasitism in the present common goldeneye population, because equation (1) is fulfilled only if r > 0:369 and the empirically estimated maximum Ar/Ao (i.e. 1.095) falls below the new threshold acceptance ratio for all r > 0:369; the empirically estimated maximum Ar/Ao crosses the new threshold acceptance ratio curve at r ¼ 0:235. Inclusion of parasitized nests that were deserted (N ¼ 19) would drastically decrease the overall value of pðCh þ Cp Þ, because in the deserted nests, pðCh þ Cp Þ is zero (see above), increasing considerably the cost of parasitism and, hence, making it less and less likely that relatedness could promote brood parasitism. I conclude that the empirically based model exercise of the present study is conservative enough in rejecting relatedness and kin selection as explanations of brood parasitism in the species. Acknowledgments I thank H. Kokko, V. Ruusila, J. Sorjonen and three anonymous referees for useful comments on the manuscript. References A˚hlund, M. & Andersson, M. 2001. Female ducks can double their reproduction. Nature, 414, 600e601. Andersson, M. 1984. Brood parasitism within species. In: Producers and Scroungers: Strategies of Exploitation and Parasitism (Ed. by C. J. Barnard), pp. 195e228. London: Croom Helm. Andersson, M. 2001. Relatedness and the evolution of conspecific brood parasitism. American Naturalist, 158, 599e614. Andersson, M. & A˚hlund, M. 2000. Hosteparasite relatedness shown by protein fingerprinting in a brood parasitic bird. Proceedings of the National Academy of Sciences, U.S.A., 97, 13188e13193. Andersson, M. & A˚hlund, M. 2001. Protein fingerprinting: a new technique reveals extensive conspecific brood parasitism. Ecology, 82, 1433e1442. Andersson, M. & Eriksson, M. O. G. 1982. Nest parasitism in goldeneyes Bucephala clangula: some evolutionary aspects. American Naturalist, 120, 1e16. Broom, M. & Ruxton, G. D. 2002. A game theoretical approach to conspecific brood parasitism. Behavioral Ecology, 13, 321e327. Bulmer, M. G. 1984. Risk avoidance and nesting strategies. Journal of Theoretical Biology, 106, 529e535. Dow, H. & Fredga, S. 1983. Breeding and natal dispersal of the goldeneye, Bucephala clangula. Journal of Animal Ecology, 52, 681e695. Dow, H. & Fredga, S. 1985. Selection of nest sites by a hole-nesting duck, the goldeneye Bucephala clangula. Ibis, 127, 16e30. Eadie, J. M. 1989. Alternative reproductive tactics in a precocial bird: the ecology and evolution of brood parasitism in goldeneyes. Ph.D. thesis, University of British Columbia.
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