J. Avian Biol. 38: 625 629, 2007 doi: 10.1111/j.2007.0908-8857.04018.x # 2007 The Authors. J. Compilation # 2007 J. Avian Biol. Received 3 July 2006, accepted 12 November 2006
Conspecific brood parasitism and egg quality in blue tits Cyanistes caeruleus Oscar Vedder, Sjouke-Anne Kingma, Nikolaus von Engelhardt, Peter Korsten, Ton G. G. Groothuis and Jan Komdeur O. Vedder (correspondence), S.-A. Kingma, P. Korsten and J. Komdeur, Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, P. O. Box 14, 9750 AA Haren, The Netherlands. E-mail:
[email protected]. N. von Engelhardt and T. G. G. Groothuis, Behavioural Biology Group, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands.
Laying eggs in nests of unrelated conspecific pairs to parasitize their parental care is a common phenomenon in birds. In blue tits Cyanistes caeruleus such conspecific brood parasitism (CBP) has never been reported in the literature. However, in a situation where breeding density was extremely high, we found six nests to be parasitized with eggs of conspecific females. Natural selection may favour elevated competitiveness of parasite young, since the negative consequences of increased sibling competition are incurred on the unrelated host parents and siblings, and therefore do not act as inclusive fitness costs for the parasites. Parasitizing females could achieve such a competitive advantage for their offspring by laying larger eggs or eggs with higher concentrations of testosterone in the yolk. We analyzed these parameters of the six parasitized nests, but did not find that parasite eggs differ systematically in these aspects from host eggs, nor that parasite eggs showed resemblance to host eggs. We suggest that a shortage of available nest sites caused some females to use CBP as a best-of-a bad job strategy, but that either the occurrence of CBP is too rare to lead to strong selection for egg adjustments or that parasitizing females are unable to do so.
In birds, laying eggs into a conspecific host nest and thereby parasitizing the parental care of other individuals is a widespread phenomenon. Such conspecific brood parasitism (CBP) is observed in at least 234 avian species (Yom-Tov 2001), and can be adopted by females as a strategy that is suboptimal compared to normal nesting but still better than not nesting at all (‘‘best-of-a-bad-job’’), or as an alternative, equally profitable, strategy to normal nesting (Davies 2000). Availability of nest sites may be a key-factor when CBP is adopted as a best-of-a-bad-job strategy, since in nestbox breeding species it is found to occur more frequently when availability of nestboxes is limited (Sandell and Diemer 1999, Saitou 2001). Young from larger or heavier eggs are known to be larger at hatching and to grow and survive better than young hatching from smaller eggs (Williams 1994, Perrins 1996, Styrsky et al. 1999). Such a size advantage in sibling competition would be particularly beneficial for parasite young because the lack of relatedness with
their nest mates and foster parents avoids the usual inclusive fitness costs of outcompeting nest mates or posing high demands on parents (Hamilton 1964). Therefore, when costs associated with producing larger eggs (Carey 1996, Monaghan and Nager 1997) are equal for parasites and hosts, the optimal level of investment in egg size is likely to be greater for parasitizing females. The same reasoning can also apply to maternal androgens in the yolk of eggs, such as testosterone. In general, it is found that young are more competitive or grow better when levels of maternal testosterone in the yolk are increased (reviewed by Groothuis et al. 2005b), but also costs of high yolk testosterone concentrations (Groothuis et al. 2005a, Mu¨ller et al. 2005, Gil et al. 2006) are reported. Therefore, also with respect to levels of maternal yolk testosterone, greater values can be expected for parasitizing females compared to nonparasitizing (host) females. The only study to date testing these predictions detected no difference in size or testosterone concentrations between parasite and host
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eggs in the European starling Sturnus vulgaris (Pilz et al. 2005). In blue tits Cyanistes caeruleus parentage analyses are frequently performed but no cases have been reported where the rearing mother could not be assigned as the genetic mother (e.g., Kempenaers et al. 1995, Krokene et al. 1998, Leech et al. 2001). However, molecular parentage analysis in our study population in The Netherlands revealed one young, out of 1032 from 100 nests in 2003, that was not mothered by the social mother (P. Korsten unpubl. data). Here we report multiple cases of CBP in the blue tit, discuss the conditions that may have led to parasitism and compare egg volume, egg mass and yolk testosterone concentrations of parasites and hosts.
Methods We conducted our fieldwork in a nestbox population of blue tits at estate ‘De Vosbergen’ (538 08?N, 068 35?E), about 10 km south of Groningen (The Netherlands), in the breeding season of 2005. The study area contains 188 nestboxes designed for blue tits and consists of 54 ha of mixed, deciduous and coniferous forest interspersed by areas of open grassland. The monitoring of the blue tit population in ‘De Vosbergen’ has started in 2001 and since then every year almost all breeding adults were caught and banded and all young were banded before fledging (for more details see Korsten et al. 2006). In the 2005 breeding season all occupied nestboxes were checked every morning, before and during the egg laying phase. Newly laid eggs were marked with an indelible marker to determine their position in the laying sequence. It is generally accepted that small passerines like blue tits maximally lay one egg each day (e.g., Perrins 1979), however, on 10 occasions in 6 nests we found two new eggs in the nest on the same day. Closer inspection of these eggs revealed that in all cases one of the eggs was distinguishable from the rest of the eggs in the clutch by the amount, size and pattern of the orange spots on the eggshell (Fig. 1). As in the closely related great tit Parus major (Gosler et al. 2000), blue tit eggshell patterns are highly repeatable within individual females (unpubl. data). Therefore we are confident that all parasite eggs were assigned as such correctly. The parasite eggs were collected, as well as the 2nd, 5th, 7th and 9th egg of the host, except from one host nest of which we only collected the 2nd and 5th egg. All eggs were collected within a day after laying and host eggs were replaced with canary-type plastic dummy eggs (dimensions: 17.7 mm 12.8 mm) to prevent desertion of clutches. Directly after collection the eggs were incubated in an incubator for three days in an attempt to obtain
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Fig. 1. Two host eggs (a and b) and two parasite eggs (c and d) that were collected from one nest. Note that the parasite eggs are reliably distinguishable from the host eggs within the nest.
DNA from the embryo. After incubation the length (L) and width (W) of each egg was measured twice to the nearest 0.1 mm using a sliding calliper, by a single observer who was blind to whether an egg was a host or a CBP egg. Egg volume (V) was calculated using the equation V 0.507 L W2 (Hoyt 1979). Egg volume was highly repeatable between the two measurements (R 0.91, F31,63 20.03, P B0.001; according to Lessells and Boag 1987), and the average of the two was used for further analyses. After taking the measurements, the eggs were individually stored in sealed plastic bags at 208 C for further analyses. Unfortunately, the attempt to obtain DNA failed because the embryos did not develop. At all nests, except for an unsuccessful one, only one female was caught feeding the young, excluding the possibility that multiple females occupied the nestbox and shared maternal care. After storage (approx. 1 month) the collected eggs were weighed to the nearest 0.0001 g using a digital balance. Testosterone concentrations were measured using a radioimmunoassay kit (DSL 4000), after extraction of testosterone from ca 250 mg yolk homogenized in 200 ml water with 3 3 ml diethylether and subsequent separation from other steroids on celite columns, with slight modifications of the protocol by
The 2005 breeding season was characterized by an extremely high density of breeding birds. There were 132 nestboxes occupied by blue tits (2.44/ha), while the average in the four preceding years was only 82 (range 56 106). This resulted in the occupation of almost all nestboxes in the area where the six parasitized nests were located. In three cases the host nest was parasitized with one egg, in two cases with two, and in one case with three eggs. The parasite eggs were all laid during the period in which the hosts were laying their 4th to 9th egg. The maximum number of parasite eggs laid in all host nests on the same day was three, suggesting that there were at least three parasitizing females in the population. Hosts laid on average 11 eggs (range 10 12), and were successful in fledging at least one young in all cases, except one. The unsuccessful host nest was deserted in the incubation phase, after clutch completion. In a nested model with a random effect of nest identity and female identity nested within nests (host or parasite), there was a random effect of female identity on yolk testosterone concentration (Ddev 17.66, P B 0.001), but not on egg volume (Ddev 3.73, P 0.05) or egg mass (Ddev 2.14, P 0.14), indicating that eggs from individual females were more similar to each other in yolk testosterone concentrations than to the eggs of other females. There was no significant random effect of nest on egg volume (Ddev 0.90, P 0.34), egg mass (Ddev 0.62, P0.43) or yolk testosterone concentration (Ddev 0.00, P1) showing that eggs laid by hosts and parasites in a common nest were not more similar to each other than to eggs of females in other nests.
Discussion Previously, CBP was thought to be absent in blue tits (Kempenaers et al. 1995). However, we found a
1.3
1.2 Egg mass (g)
Results
When type of egg was included as a fixed effect, parasite eggs did not significantly differ from host eggs in volume (Ddev 1.12, P0.29), mass (Ddev 1.14, P 0.29, Fig. 2a), or yolk testosterone concentration (Ddev 0.58, P 0.45, Fig. 2b). All analyses repeated with egg width and egg length separately also showed no significant effects (all P 0.10).
1.1
1.0
0.9 Host
b
Testosterone (pg/mg yolk)
Schwabl (1993); see Eising et al. (2001). Recoveries were assessed in individual samples (on average 52%). Samples were assayed in two assays, intra-assay variation was 9%, inter-assay variation was 3.4%. Differences between parasite and host eggs were tested with hierarchical linear models in the MLwiN program, version 2.0 (Rasbash et al. 2000). Dependent variables were egg volume, egg mass and yolk testosterone concentration. Type of egg (parasite or host) was entered as a fixed factor. Random effects were modelled in a hierarchical way and concerned nest, female identity (parasite or host, assuming that all parasite eggs within a nest originated from a single female) and individual egg, respectively. This way we accounted and tested for non-independence of eggs laid by different females in different nests. Significance of fixed and random effects was tested in models using maximum likelihood estimation by calculating the increase in deviance (Ddev) when the variable was removed from a model, which follows a x2 distribution.
Parasite
20
15
10
5
0 Host
Parasite
Fig. 2. Average host and parasite values for egg mass (a) and yolk testosterone concentration (b) per nest. The dashed lines connect the host and parasite values for each nest.
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conspecific eggs appearing in the middle of the laying sequence that could not be attributed to the female that occupied the nestbox. This implies that at least certain females are capable of laying their eggs in an occupied nestbox and therefore not constrained to use CBP as a potentially adaptive strategy. We believe that our observations are not mere accidents such as failed take-over attempts. Nestbox take-overs do occur in our study area but do not fit the pattern observed here, because they often result in the death of the host and always result in the subsequent building of a new nest over the original clutch and the start of laying a new clutch at least several days later (personal observations by OV and SK). Therefore a failed take over attempt would not result in additional eggs. In addition, the fact that in some cases host nests received multiple parasite eggs over consecutive days, excludes the possibility of an one-time accidental dump laying of an egg. The fact remains that although the species is intensively studied, daily nest visits in the laying phase or molecular parentage analyses never revealed cases of CBP before (e.g., Kempenaers et al. 1995, Krokene et al. 1998, Leech et al. 2001). So, if blue tits are capable of laying eggs into conspecific host nests, why does it not occur more frequently? Since we were not able to identify the parasitizing females we can not exclude the possibility that these females also raised offspring in a nest of their own and compare reproductive success of normal and parasitizing females. CBP may therefore be as profitable as, or even more profitable than, the normal mating strategy (e.g., A˚hlund and Andersson 2001). However, its rarity may be best explained by the possibility that CBP only is profitable for females that can not acquire a nest site. Even if CBP has a net pay-off in fitness lower than normal breeding, CBP may at least give females without a nest site some chance of getting offspring as a best-of-a-bad-job strategy. This is experimentally supported by a study in grey starlings Sturnus cineraceus , which showed that the level of parasitism decreased with the number of available nestboxes (Saitou 2001). Therefore, the widespread practice of putting up an excess of nestboxes in most blue tit study populations may lower the frequency of CBP by decreasing nest site competition among females. Indeed, van Balen et al. (1982) found that there was more competition, among various cavity nesting birds, over nest sites in areas without nestboxes compared to areas with nestboxes and numerous studies report an immediate increase in breeding numbers when (more) nestboxes are provided, suggesting the availability of nest sites to be limiting the numbers of breeding pairs (reviewed by Newton 1994). Hence, CBP might be much more common in blue tit populations in a more natural habitat, where no nestboxes are available. Our finding of CBP in a situation of extremely high breeding
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density, which caused a lack of available nestboxes in some areas, fits this hypothesis. In agreement with a study on brood parasitic European starlings (Pilz et al. 2005), we did not find that parasite eggs were larger, heavier or contained higher concentrations of yolk testosterone than host eggs. If CBP is as rare in blue tits as reported from nestbox studies, selection to favour increased competitiveness in parasite young might simply be too weak to have led to such adaptations. Another possibility is that the investment in greater egg mass or yolk testosterone concentration is too costly for the parasitizing female, the parasite young, or both. There is ample evidence that investment in egg mass is costly for females (Carey 1996, Monaghan and Nager 1997), and recently also costs have been recognized of high yolk testosterone concentrations for immunocompetence of both females (Gil et al. 2006) and young (Groothuis et al. 2005a, Mu¨ller et al. 2005). Since females that resort to CBP are likely to be outcompeted individuals, these females may be of lower quality than hosts and therefore unable to bear the costs of greater investment in egg volume, egg mass or yolk testosterone. In conclusion, we report for the first time the occurrence of CBP in blue tits. Our results suggest that parasitizing females produce eggs that do not differ substantially and systematically from their host eggs. Future studies may aim at inducing parasitism, perhaps by removing nestboxes, in such a way that parasite and non-parasite eggs laid by the same female can be compared (e.g., Lyon 1993). This would control for possible quality differences between parasites and hosts that may obscure differences in egg investment. Acknowledgements We thank Bonnie de Vries and Maarten Gasthuizen for assistance in analysing yolk testosterone concentrations. Comments of Sandra Bouwhuis, Michael Magrath and two anonymous referees greatly improved the manuscript. All field procedures were approved by the Animal Experiments Committee (DEC) of the University of Groningen.
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