Behavioral Ecology Advance Access originally published online on February 15, 2006
Behavioral Ecology 2006 17(3):459-465; doi:10.1093/beheco/arj049
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Public information and conspecific nest parasitism in goldeneyes: targeting safe nests by parasites
Finnish Game and Fisheries Research Institute, Joensuu Game and Fisheries Research, Yliopistokatu 6, FIN-80100 Joensuu, Finland
Address correspondence to H. Pöysä. E-mail: hannu.poysa{at}rktl.fi.
Received 21 December 2004; revised 13 December 2005; accepted 16 January 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Conspecific nest parasitism (CNP) is a widespread alternative reproductive tactic in birds. Several hypotheses have been put forward to explain the evolution and occurrence of CNP, but no generally applicable hypothesis exists. Recent experimental results from the common goldeneye (Bucephala clangula), a cavity-nesting duck, have revealed that parasitic females preferentially lay eggs in safe nest-sites, implying that nest predation risk is an important ecological determinant of CNP. The present study focuses on the mechanisms by which parasites identify safe nest-sites. Predation risk of a given nest-site was predictable between successive breeding seasons. At the end of the nesting season, females prospected active nest-sites more frequently than nest-sites that did not have a nest in the current season. Nest-sites that had been prospected more frequently by females in year t had a higher probability to be parasitized in year t + 1. The results suggest that the use of public information, derived through nest-site prospecting, enabled parasites to target safe nests. These findings provide a new and potentially generally applicable perspective to understand the evolution and occurrence of CNP.
Key words: common goldeneye, conspecific nest parasitism, nest predation risk, nest-site prospecting, public information.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Conspecific nest parasitism (CNP) is an alternative reproductive tactic in which a female lays eggs in the nest of a conspecific female that incubates the eggs and raises the young. It is a widespread reproductive tactic in birds (Arnold and Owens, 2002
; Davies, 2000; Geffen and Yom-Tov, 2001; Yom-Tov, 2001). An equivalent reproductive trait, more generally phrased as conspecific brood parasitism or egg dumping, occurs in other animal taxa, including fishes, amphibians, and insects (e.g., García-González and Gomendio, 2003; Sato, 1986; Summers and Amos, 1997). Also, many parallels between birds and some insects in the patterns of CNP have been identified (Brockmann, 1993; Field, 1992). Several hypotheses have been proposed to explain the evolution and occurrence of CNP (reviews in Eadie et al., 1988; Petrie and Møller, 1991; Sayler, 1992), but few studies have tried to test alternative hypotheses, and no generally applicable hypothesis exists (see also Arnold and Owens, 2002). Recent theoretical work has focused especially on the possible role of relatedness and kin selection in the evolution of CNP (Andersson, 2001; López-Sepulcre and Kokko, 2002; Zink, 2000). However, both model predictions (Andersson, 2001; Zink, 2000) and empirical findings (Andersson and Åhlund, 2000; Pöysä, 2004; see also Lyon and Eadie, 2000; Semel and Sherman, 2001) of the role of relatedness in the evolution of CNP are contradicting. Also, the dynamics and equilibrium level of CNP within populations has received theoretical attention (Eadie and Fryxell, 1992; Nee and May, 1993).
Recent field experiments done at two spatial scales have revealed that parasitic egg laying is associated with nest predation risk in the common goldeneye (Bucephala clangula), a cavity-nesting precocial duck in which nest-site fidelity is high (Dow and Fredga, 1983) and CNP is particularly frequent (Eadie, 1989; Eriksson and Andersson, 1982; Pöysä, 1999). First, in an experimental setting of real nests, Pöysä (1999) found that nests parasitized in a given year were more frequent in those nest-sites that were not depredated during the previous nesting attempt in earlier years than in nest-sites that were depredated. Second, in an experiment with dummy nests, controlling for host identity and quality, Pöysä (2003a) found that parasites preferred to lay in the experimental boxes on lakes where real nest predation risk was low. These two experimental results support the hypothesis that nest predation risk is an important ecological determinant of CNP. In contrast to the old risk spreading hypothesis which assumes that nests are predated at random and parasites lay randomly (Bulmer, 1984; Rubenstein, 1982), the new nest predation risk hypothesis is based on the assumption that nest predation risk is nonrandom and parasites lay accordingly (Pöysä, 1999, 2003a).
The critical question then is how do parasites recognize safe nest-sites? Nest-site prospecting has been considered as an important element of nest-site selection in goldeneyes, that is, at the end of the breeding season females visit potential nest-sites for the following year (Eadie and Gauthier, 1985; Pöysä et al., 1999; Zicus and Hennes, 1989). By doing so, females could obtain information of the past history of the nest-site by detecting the presence of eggshell fragments and membranes in hatched nests (Eadie and Gauthier, 1985). Extending this idea, Pöysä (1999, 2003a) suggested that prospecting could be a behavioral mechanism by which parasites get information on nest-site–specific predation risk. Prospecting for breeding sites is a widespread behavioral trait in birds, and it has been observed in other taxa too (Danchin et al., 2001, 2004; Reed et al., 1999). In particular, prospecting has been identified as a general way of gathering public information, that is, information derived from the performance of conspecifics (Danchin et al., 2001, 2004). Public information has been recognized more and more important in individual decision making related, for example, to foraging-patch choice (Valone and Giraldeau, 1993), the choice of breeding colony or site (Brown et al., 2000; Danchin et al., 1998; Doligez et al., 2002), and mate choice (Nordell and Valone, 1998; additional examples in Danchin et al., 2004). In particular, the use of public information has been considered important in breeding habitat selection in several species, the common goldeneye serving as one example (review in Danchin et al., 2001). However, neither prospecting (but see Pöysä, 1999, 2003a) nor public information has previously been connected with CNP.
In this paper, I put forward a new hypothesis by proposing that public information may play an important role in CNP. First, I study whether nest-site–specific predation risk is predictable over time, a crucial but rarely tested assumption of the public information idea (Danchin et al., 2001; Doligez et al., 2003). Second, I demonstrate that, at the end of the breeding season, common goldeneye females frequently prospect for nest-sites and that prospecting is more frequent at active nest-sites than at nest-sites that were not used in the current season. Third, I examine whether nest-sites that were prospected more frequently in year t were parasitized more frequently in year t + 1.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The study was conducted in southeast Finland (61° 35' N, 29° 40' E) in the breeding seasons 1999–2003. The 8 x 12–km study area is dominated by pine (Pinus sylvestris) or mixed (pine, birch Betula spp., and spruce Picea abies) forests interspersed with lakes of varying size (mean = 3.7 ha, range = 0.2–24.0 ha, n = 35 lakes). New nest-boxes were erected in the study area for common goldeneyes between 1992 and 1994, and the total number of nest-boxes available each year between 1999 and 2003 was 64–67 (see Pöysä, 1999
; Pöysä H and Pöysä S, 2002).
Nest-site–specific predation risk and breeding history
All nest-boxes were frequently checked from late April through June in each year for nesting attempts (at least one egg laid) and to determine the fate of each nesting attempt, that is, successful (at least one duckling departed the nest-box), deserted (clutch deserted during egg laying or incubation), or depredated (clutch depredated during egg laying or incubation, that is, all eggs were taken [this usually was the case] or at least one egg disappeared and the nest was deserted; see also Pöysä, 1999). Width and length of new eggs were measured on each visit. Nest predation is high and the main determinant of nesting success in the present common goldeneye population (Pöysä, 1999; Pöysä et al., 1997, 2001a; Pöysä H, unpublished data). To study the predictability of predation risk in a given nest-site, I randomly selected for each nest-box two successive years when there was a nesting attempt in the nest-box in both years. Each nest-box was classified into one of the following four categories: depredated in both years, nondepredated in both years, depredated in year 1 but nondepredated in year 2, and nondepredated in year 1 but depredated in year 2. As one random selection per nest-box and associated test may lead to a misleading conclusion (Danchin et al., 1998), I repeated the random resampling of two successive years per nest-box 100 times to obtain the distribution of p value and test statistic (see below).
Measuring nest-site prospecting
At the end of the nesting period during 1999–2002, a nest-site prospecting study was done to measure the frequency of prospecting at nests of different fate. In each year, two sets of nest-box pairs were used. In the first set (hereafter set 1), one of the nest-boxes (control nest-box) did not have a nesting attempt in that year but was an acceptable nest-box (i.e., had at least one nesting attempt in some previous year since 1992), whereas the other nest-box had a successful nesting attempt in that year. In the second set (hereafter set 2) of nest-box pairs, one of the nest-boxes was a control nest-box (same criteria as in set 1), and the other nest-box had a nesting attempt that was either deserted or depredated in that year (hereafter called unsuccessful nest-boxes). The prospecting study was run for five consecutive days for each pair of nest-boxes, that is, the control and the successful nest-box of a given nest-box pair in set 1 was followed during the same 5 days in a given year, and, similarly, the control and the unsuccessful nest-box of a given nest-box pair in set 2 was followed during the same 5 days in a given year. The study was done between 18 June and 4 July in 1999, between 2 and 14 June in 2000, between 5 and 24 June in 2001, and between 11 and 25 June in 2002. In the nest-box pairs of set 1, the prospecting study started 1–16 days (mean 4.5 days) after the brood left the successful nest-box, and in the nest-box pairs of set 2, the prospecting study started 1–40 days (mean 17.4 days) after the unsuccessful nest-box was deserted or depredated (possible intact eggs left were removed from the nest-boxes before the prospecting study started).
To measure the nest-box–specific prospecting rate, I put in the middle of the bottom of the nest-box a 9.5 x 10–cm paper tray with a small hole in the middle. In the hole of the tray, I placed a broken chicken egg dyed to mimic the color of goldeneye eggs (similar broken eggs as used by Pöysä, 2003a). Broken egg was used only as a convenient method of detecting whether a visit by a common goldeneye female has occurred, not to simulate a particular stimulus to visiting birds; a similar broken egg was used in control, successful, and unsuccessful nest-boxes, so it did not cause any bias in the comparisons between box types. When common goldeneye females visit a nest-box, they sit on the bottom and scratch the nest material. Hence, the visit of a female in a nest-box was easy to recognize as the broken egg was split into small pieces, and the paper tray was wrinkled and usually moved near the wall of the nest-box. This was verified in the field by checking nest-boxes immediately after the prospecting female left the nest-box. During the 5-days experimental period, I checked each nest-box once per day for possible common goldeneye visits, that is, nest-box–specific prospecting rate ranged from 0 (no visits at all) to 1.0 (nest-box visit by one or more females was recognized on each of the 5 days). When I checked the nest-boxes, I restored the setting when necessary and replaced the broken egg if it was smashed to pieces. Each nest-box was used only once in the analyses, as a control (in set 1 or 2), successful, or unsuccessful nest-box.
Successful common goldeneye females do not visit their own nest after the brood has left it, not even in those cases when one or more ducklings have remained in the nest-box (Sirén, 1956; Pöysä H, unpublished data; see also Pöysä, 2004). Common goldeneye males do not visit the nests at all. In the present study area, two small hole-nesting passerines, the great tit (Parus major) and the redstart (Phoenicurus phoenicurus), are potential visitors of common goldeneye nest-boxes at the time of the prospecting study, but these species hardly leave any visible marks of their visits in the nest-box (i.e., the broken chicken egg on the paper tray and the nest material remain untouched). The pine marten (Martes martes) is the main predator of common goldeneye nests in the present study area (Pöysä et al., 1997). To study how frequently pine martens visited the nest-boxes during the prospecting study and what kind of marks they leave in the nest-box, I put an intact chicken egg in some of the nest-boxes during the prospecting study in 2000, 2001, and 2002 (an intact chicken egg was kept for 98 nest-box days in 22 different nest-boxes; intact chicken eggs have been successfully used in nest predation experiments in the common goldeneye, see Pöysä, 1999, 2003a; Pöysä et al., 1997, 2001a). When I inspected these boxes, neither a common goldeneye nor a pine marten had visited the nest-box in 56 cases (both the broken egg on the paper tray and the intact egg were untouched); in 41 cases, the nest-box was visited by a common goldeneye but not by a pine marten (marks of a common goldeneye visit were clear [see above] but the intact egg was untouched; referred to as "intact-egg-present" visits by common goldeneye females in logistic regression analysis below); and in 1 case, the nest-box was visited by a pine marten but not by a common goldeneye (broken egg on the paper tray was untouched but the intact egg was depredated). Additional tests in an identical setting confirmed that, indeed, the broken chicken egg remains untouched during a predatory visit by a pine marten in the nest-box (four cases; Pöysä H, unpublished data). In other words, a visit by a pine marten in a nest-box is easily distinguished from a visit by a common goldeneye, and, all in all, visits by pine martens in the nest-boxes were infrequent. In conclusion, visits by other animals other than common goldeneye females do not confuse the measuring of prospecting rate.
Identification of parasitized nests
Parasitized nests were identified using two methods: (1) more than 1 egg laid within 24 h (Eadie, 1989; MacWhirter, 1989) and (2) within-clutch variation of egg width, length, and weight (weights were calculated using the formulae developed by Rohwer, 1988 for waterfowl) exceeded a threshold value (maximum Euclidean distance [MED] between any two eggs within a clutch), a method developed by Eadie (1989) for goldeneyes. A nest was considered parasitized if MED > 3.0 (Pöysä et al., 2001b). The latter method has been tested further in the common goldeneye by Pöysä et al. (2001b; see also Pöysä, 1999, 2003a,b, 2004) and Ådahl et al. (2004). The methods give highly comparable results in the present population (Pöysä, 1999, 2003b). In addition, a comparison based on protein fingerprinting to identify eggs of different females (see Andersson and Åhlund, 2001) confirmed that, indeed, the method based on within-clutch MED value is reliable enough to identify parasitized nests (clutches laid by one female only: mean MED = 1.38, 95% confidence intervals [CI] = 1.07–1.70, n = 14; clutches laid by more than one female: mean MED = 3.48, 95% CI = 2.80–4.16, n = 12; Pöysä H, Lindblom K, Rutila J, and Sorjonen J, unpublished data from 2001 to 2003).
To study whether the occurrence of parasitism in a given nest-box in year t + 1 is associated with nest-box–specific prospecting rate in year t, I included all nesting attempts (at least one egg laid) that were exposed to parasitism for more than 5 days in year t + 1. Exposure time was measured as follows: for successful nests and for nests depredated or deserted during the incubation phase: from the appearance of the first egg until the start of incubation; for nests deserted during the egg-laying period: from the appearance of the first egg until the appearance of the last egg (egg laying in one of these nests stopped after the second egg, and the nest was not depredated before I removed the eggs 31 days after the desertion; hence, this nest got an exposure time of 1 day); and for nests depredated during the egg-laying phase: from the appearance of the first egg until the last visit to the nest, before it was depredated. The criterion of more than 5 days is conservative but minimizes the risk of misidentifying as nonparasitized those nests that were depredated later in the laying phase. In an experiment comparing the occurrence of nest parasitism in decoy nests and real common goldeneye nests (Pöysä, 2003b), the first parasitic egg in the real nests was laid, on average, 4.9 days (range 2–10 days, n = 13 nests that proceeded to incubation) after the appearance of the first host egg, and some of the decoy nests were parasitized on the first day of exposure.
Statistical methods
Predictability of the fate of a nesting attempt in a given nest-box between years t and t + 1 was measured with Yule's coefficient of association, Q (Zar, 1996, p. 398; range from –1 to +1). Because one of the expected cell frequencies consistently was less than five, I used Fisher's Exact test to test for the significance of Yule's Q. I calculated the value of Q and Fisher's Exact p for each of the 100 random samples (see above) and calculated 95% CI for them to determine the statistical significance of the association. Specifically, if the higher value of the 95% CI of the Fisher's Exact p values was <.05, then the predictability of the fate of nesting attempts in the nest-boxes was significant (see Danchin et al., 1998). Differences in prospecting rate by common goldeneye females between different types of nest-boxes were tested with Mann-Whitney U test. I used logistic regression to study whether the probability of a given nest (nest-box) to be parasitized in year t + 1 depends on the prospecting rate by common goldeneye females in the same box in year t. The analysis was performed as a backward stepwise (p to remove = .05) procedure by including prospecting rate, number of intact-egg-present visits by common goldeneye females in year t (see Measuring Nest-Site Prospecting), and exposure time in year t + 1 as explanatory variables (main effects only). Note that the number of intact-egg-present visits by common goldeneye females and the exposure time were included only to control for their possible confounding effect on the occurrence of parasitism. Test statistics for each explanatory variable before removal from the model and for the final model will be given. Statistical analyses were conducted using SYSTAT 10.0 software. All significance levels are for two-tailed tests.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The fate of a nesting attempt in a given nest-box was highly predictable between years t and t + 1. In the set of 100 random samples of two successive years per nest-box (n = 27 nest-boxes in all), on average, in 73.3 ± 4.1% (SD) of cases the fate was the same between successive years (depredated [mean ± SD = 7.5 ± 0.6] or nondepredated [mean ± SD = 12.3 ± 1.1] in both years), whereas only in 26.7 ± 4.1% (SD) of cases it was different (depredated in year t but not in year t + 1 [mean ± SD = 1.0 ± 0.8] or vice versa [mean ± SD = 6.2 ± 1.1] [mean of Yule's Q = 0.878, 95% CI = 0.859–0.898; mean of Fisher's Exact p = .024, 95% CI = 0.018–0.031]).
Prospecting rate by common goldeneye females was higher in active nest-boxes than in their control boxes (Figure 1; successful versus control 1: U = 16.5, p < .001; unsuccessful versus control 2: U = 13.0, p = .030). Moreover, prospecting rate was higher in successful than in unsuccessful nest-boxes (U = 20.0, p = .006). Considering successful nest-boxes, timing of the start of the prospecting study with respect to brood departure (see Measuring Nest-Site Prospecting) did not affect prospecting rate: prospecting rate versus date (in June) of the start of the prospecting study, rs = –.045, p > .50, n = 16; prospecting rate versus number of days from brood departure until the start of the prospecting study, rs = –.082, p > .50, n = 16. Both successful and unsuccessful nest-boxes were studied in each year between 1999 and 2002, and there was no difference in the timing of the start of the prospecting study between these boxes in any year (Mann-Whitney U tests; p > .16 in all comparisons).
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Fitting the three explanatory variables in a backward stepwise logistic regression revealed that the number of intact-egg-present visits by common goldeneye females in year t (
2 = 0.676, p = .411, df = 1) and the exposure time in year t + 1 (2 = 0.456, p = .499, df = 1) had no influence on the probability of parasitism in year t + 1. Hence, the presence of an intact chicken egg in the nest-box in year t to recognize possible pine marten visits (see Measuring Nest-Site Prospecting) and the exposure time in year t + 1 did not confound the occurrence of parasitism in year t + 1. Of the three explanatory variables included, only prospecting rate by common goldeneye females in year t significantly influenced the probability of a nest (nest-box) to be parasitized in year t + 1 (2 = 7.868, p = .005, df = 1). The final model including the prospecting rate only was highly significant: the higher the prospecting rate in year t the higher the probability of parasitism in year t + 1 (Figure 2; log-likelihood G = 14.045, p < .001, df = 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The occurrence of parasitism in a given nest-site was associated with prospecting rate in the same site the previous year. This is a new and important finding, not only in the common goldeneye but also in the context of CNP in general. Pöysä (1999)
found that nests parasitized in a given year were more frequent in those nest-sites that were not depredated during the previous nesting attempt than in nest-sites that were depredated. Similarly, considering the 29 nest-sites studied here for the association between the occurrence of parasitism and prospecting rate (i.e., the nest-sites in Figure 2), the proportion of parasitized nests in year t + 1 was higher in nest-sites that were successful in year t (84.6%, n = 13) than in nest-sites that were unsuccessful in year t (43.8%, n = 16; Williams' corrected G = 5.254, p < .05, df = 1). These findings together provide strong support for the hypothesis that the use of public information through nest-site prospecting most probably is the mechanism behind the disproportional occurrence of parasitism in safe nest-sites.
It is emphasized that nest-site limitation (Eadie, 1991) and host-parasite relatedness (Andersson and Åhlund, 2000), factors that also have been suggested to explain the occurrence of CNP in the species, have been ruled out as determinants of CNP in the present population (Pöysä, 1999, 2003a,b, 2004). Also it should be noted that, in the present study, only those nest-sites that had a nesting attempt in year t + 1 could be used to test for the association between nest-site prospecting rate in year t and the occurrence of CNP in year t + 1. There were 54 other cases (33 nest-boxes; prospecting rate measured, on average, in 1.6 years per nest-box) in which prospecting rate was measured in year t but there was no nesting attempt in year t + 1. In five of these cases, the prospecting rate was as high as 0.6–0.8. These observations imply that high prospecting rate associated with parasitic laying, as demonstrated here, cannot be interpreted as competition for high-quality nest-sites; otherwise, the frequently prospected nest-sites should have been used for nesting in year t + 1 by some of the prospecting females. Similarly, the egg-laying patterns of individual parasitic females in a Swedish common goldeneye population suggest that competition for nest-sites does not explain CNP in the species (Åhlund and Andersson, 2001).
The value of public information depends, among other things, on the predictability of the environment over time, that is, public information should allow individuals to predict their own success (Danchin et al., 2001; Doligez et al., 2003). The occurrence of nest predation in a given nest-box proved to be predictable from 1 year to the next in the common goldeneye. This finding is in line with Pöysä (1999) who demonstrated that predation risk was not randomly distributed among nest-sites over time and space. Similarly, Pöysä (2003b) showed that the ranking of lakes in terms of nest predation risk was consistent over longer time periods. The finding of the present study is particularly important in that it demonstrates the predictability of nest predation risk between consecutive breeding seasons. If parasites can correctly assess the predation risk of a given nest-site in year t they are able to target right nests in year t + 1.
Common goldeneye females prospected nest-sites that had a nest (successful or not) during the current year more frequently than control nest-sites that did not have a nest. Furthermore, boxes with a successful nest were prospected more frequently than those with an unsuccessful nest. Similarly, Zicus and Hennes (1989) found in the same species that prospecting rate of females was higher in successful nest-boxes than either in those having an unsuccessful nest or those that were unused in the current year. Hence, prospecting by common goldeneye females appears to be directed at active nests, especially successful ones during the same season. These are the nests that provide the useful information for females that lay parasitically in the coming season, that is, eggshell fragments and membranes revealing successful (safe) nests (Eadie and Gauthier, 1985; Zicus and Hennes, 1989). In the wood duck (Aix sponsa), these remnants are so conspicuous that they can be used to estimate the number of hatched ducklings (Davis et al., 1998). It is important to note that successful common goldeneye females usually return to nest in the same box next year (Dow and Fredga, 1983; Eadie et al., 1995; Savard and Eadie, 1989), hence providing a nest to be parasitized. These traits make the use of public information a profitable strategy to identify and utilize safe nest-sites by parasites.
I did not identify the breeding status of the prospecting females. Zicus and Hennes (1989) found that prospecting was practiced by unsuccessful nesters, yearling nonnesters, and even females that had a brood. In the kittiwake (Rissa tridactyla), prospectors (squatters) were identified mostly as prebreeders and failed breeders, the frequency of prospecting being lowest in successful breeders (Cadiou et al., 1994). However, unlike in the common goldeneye, in this species prospecting is practiced by both females and males. Considering the high nest-site fidelity of successful common goldeneye females (Dow and Fredga, 1983; Eadie et al., 1995; Savard and Eadie, 1989), prospecting by brood hens is unexpected if nest-site selection is the sole function of prospecting (see also Eadie and Gauthier, 1985). Zicus and Hennes (1989) suggested that females with broods would profit from nest prospecting because of the probable loss of some cavity trees from year to year, that is, a successful female may lose her nest-site and therefore needs to be aware of other sites in the area. However, it remains unclear why brood hens should not be able to get this information earlier in the season (e.g., during egg laying) but prospect after the broods have left the nest-sites. An alternative explanation why brood hens, in addition to nonbrood hens, prospect nest-sites at the end of the nesting season is that they are looking for potential and safe target nests in order to lay parasitic eggs in the next season. Common goldeneye females may change from normal nesting to parasitic laying between years, and some females may lay their own clutch and parasitize other females within the same season (Åhlund and Andersson, 2001; Eadie, 1989). Together, these observations suggest that evolutionary functions of nest-site prospecting in goldeneye females are twofold, at least. First, as previously suggested (Eadie and Gauthier, 1985; Pöysä et al., 1999; Zicus and Hennes, 1989), prospecting behavior is an important element in the process of nest-site selection. Second, based on the present results, I suggest that nest-site prospecting provides parasitic females with information that enables them to target parasitic laying profitably in the coming breeding season should they choose to use that strategy. The use of public information seems to be an important element in both of these functions.
The present study design did not enable the identification of prospectors. It was therefore not possible to confirm if the females that prospected a given nest-site were really the same females that came back the next year to parasitize that nest. Alternatively, prospectors could have been solitary females that were looking for a nest-site and built a nest in these same boxes the next year and, hence, served as hosts to other parasitizing females. Several lines of evidence suggest that this is an unlikely explanation. First, although prospecting in the common goldeneye no doubt is associated with nest-site selection (see above), all prospecting events seem not to have this function. As already mentioned above, some nest-sites that were prospected at a very high rate in year t were not occupied at all in year t + 1. Because successful (therefore obviously preferred) nest-sites in particular were prospected at a high rate, those nest-sites should have been occupied in year t + 1 by some of the prospectors if prospecting mainly was for nest-site selection. Second, nest-sites that have been successful in year t usually remain unoccupied by new females in year t + 1 in case the successful female does not come back the next year. This was confirmed by our data from two other common goldeneye populations in which we have banded and recaptured all nesting females each year (Maaninka, see Ruusila et al., 2001; Evo, see Paasivaara and Pöysä, 2005). In Maaninka, a nest-site that had been successful in year t but not occupied by the same female in year t + 1 remained unoccupied in 78.3% of cases (n = 258; Runko P, unpublished data from 1985 to 2004), the corresponding figure being 85.3% (n = 68) in Evo (Pöysä H, unpublished data from 1992 to 2004). Third, Eadie and Gauthier (1985) report that, indeed, some of the common goldeneye females that prospected nest-sites in year t nested near these sites in year t + 1. However, none of these females that nested (five in all) did nest in those sites where they were trapped as prospectors the previous year. Eadie and Gauthier (1985) mention that several females were repeatedly caught at the same nest-site as prospectors, so trapping evidently did not deter the females from returning to nest in the prospected nest-sites. Given that some females both parasitize and lay their own clutch within the same season (Åhlund and Andersson, 2001; Eadie, 1989), the prospecting females that returned to nest in year t + 1 may have laid parasitically in the nest-sites they visited in year t. Nest-sites that were prospected in year t did have a successful or deserted nesting attempt that year but, unfortunately, the authors do not report the status of the nest-sites in year t + 1, especially if the prospected nest-sites were parasitized or not. At any rate, these observations imply that prospecting a given nest-site by a particular female does not necessarily result in nest building by that female in the site the next year.
The results of the present study put into a new perspective the findings of the general occurrence of CNP. Recent analyses taking into account phylogenetic relationships of species have revealed that cavity nesting and colonial breeding are associated with high rates of CNP (Beauchamp, 1997; Geffen and Yom-Tov, 2001; see also Eadie et al., 1988; Yom-Tov, 2001). Furthermore, by combining results from several studies on waterfowl, Eadie et al. (1998) found that frequencies of CNP within populations of cavity-nesting species were higher than in ground-nesting species that nest in emergent vegetation or in upland areas, that is, use nest-sites that are more difficult to find by parasites and not repeatedly used. Hence, based on the current knowledge, both nest-site prospecting (Danchin et al., 2001; Reed et al., 1999) and CNP (Beauchamp, 1997; Geffen and Yom-Tov, 2001) are particularly frequent among cavity-nesting and colonial-breeding species. An additional feature in common among these species is that the same nest-sites (cavities, cliffs, etc.) are used for several years, enabling the nest-site–specific information of success gathered in year t to be profitably used by parasites in year t + 1. The common goldeneye studied here is a representative of noncolonial cavity-nesting species. A good candidate from colonial-breeding species is the cliff swallow (Petrochelidon pyrrhonota) in which CNP is common and parasites seem to assess the quality of potential hosts and nest-sites (Brown and Bomberger Brown, 1988, 1991) and in which the use of public information in breeding site selection may occur (Brown et al., 2000).
In conclusion, the use of public information gained in nest-site prospecting enables parasitic common goldeneye females to lay eggs in safe nests. I hypothesize that, in general, linking the idea of public information to CNP provides a new key to understand the disproportional occurrence of this alternative reproductive tactic in birds. The traditional risk spreading hypothesis based on random nest predation (Rubenstein, 1982) may not explain the evolution of CNP (Bulmer, 1984). However, nonrandom nest predation risk or failure due to some other reason, coupled with the ability of parasites to assess the site-specific risk by using public information, should promote the evolution of CNP. Future studies addressing the evolution and ecological determinants of CNP should scrutinize this new hypothesis. Also, as there seems to be many interesting similarities between birds and insects, especially Hymenoptera in the patterns of CNP (Brockmann, 1993; Field, 1992; see also Zink, 2000), it would be interesting to explore whether the new hypothesis put forward here also helps to explain the evolution and occurrence of CNP in invertebrates.
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ACKNOWLEDGEMENTS |
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I thank Naomi Pierce, Vesa Ruusila, Jorma Sorjonen, and two anonymous referees for valuable comments on the manuscript.
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REFERENCES |
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