Cooperation and conflict in conspecific brood parasitism : an alternative reproductive tactic

Interactions among individuals give rise to both cooperation and conflict. Individuals will behave selfishly or altruistically depending on which gives the higher payoff. The reproductive strategies of many animals are flexible and several alternative tactics may be present from which the most suitable one is applied. Generally, alternative reproductive tactics may be defined as a response to competition from individuals of the same sex. These alternative reproductive tactics are means by which individuals may fine-tune their fitness to the reigning circumstances and which are shaped by the environment individuals are occupying as well as by the behaviour of other individuals sharing the environment. By employing such alternative ways of achieving reproductive output, individuals may alleviate competition from others. Conspecific brood parasitism (CBP) is an alternative reproductive strategy found in several egg laying animal groups, and it is especially common among waterfowl. Within this alternative reproductive strategy, four reproductive options can be identified. These four options represent a continuum from low reproductive effort coupled with low fitness returns, to high reproductive effort and consequently high benefits. It may not be evident how individuals should allocate reproductive effort between eggs laid in their own nest vs. in nests of others, however. Limited fecundity will constrain the number of eggs donated by a parasite, but also the tendency for hosts to accept parasitic eggs may affect the allocation decision. Furthermore, kinship, individual quality and the costs of breeding may play a role in complicating the allocation decision. In this thesis, I view the seemingly paradoxical effects of kinship on conflict resolution in the context of alternative reproductive tactics, examining the resulting features of cooperation and conflict. Conspecific brood parasitism sets the stage for investigating these questions. By using both empirical and theoretical approaches, I examine the nature of CBP in a brood parasitic duck, the Barrow's goldeneye (Bucephala islandica). The theoretical chapter of this thesis gives rise to four main conclusions. Firstly, variation in individual quality plays a central role in shaping breeding strategies. Secondly, kinship plays a central role in the evolution of CBP. Thirdly, egg recognition ability may affect the prevalence of parasitism. If egg recognition is perfect, higher relatedness between host and parasite facilitates CBP. Finally, I show that the relative costs of egg laying and post-laying care play a so far underestimated role in determining the prevalence of parasitism. The costs of breeding may outweigh possible inclusive fitness benefits accrued from receiving eggs from relatives. Several of the patterns brought out by the theoretical work are then confirmed empirically in the following chapters. Findings include confirmation of the central role of relatedness in determining the extent of parasitism as well as inducing a counterintuitive host clutch reduction. Furthermore, I demonstrate a cost of CBP inflicted on hosts, as well as results suggesting that host age reflects individual quality, affecting the ability to overcome costs inflicted by CBP. In summary, I demonstrate both theoretically and empirically the presence of cooperation and conflict in the interactions between conspecific parasites and their hosts. The field of CBP research has traditionally been divided, but the first steps have now been taken toward the acceptance of the opposite side of the divide. Especially the theoretical findings of chapter 1 offer the possibility to view seemingly contrasting results of various studies within the same framework, and may direct future research toward more general features underlying differences in the patterns of CBP between populations or species.

Current brood size and residual reproductive value predict offspring desertion in the burying beetle Nicrophorus vespilloides

Life-history theory suggests that offspring desertion can be an adaptive reproductive strategy, in which parents forgo the costly care of an unprofitable current brood to save resources for future reproduction. In the burying beetle, Nicrophorus vespilloides, parents commonly abandon their offspring to the care of others, resulting in female-only care, male-only care, brood parasitism, and the care of offspring sired by satellite males. Furthermore, when there is biparental care, males routinely desert the brood before larval development is complete, leaving females behind to tend their young. We attempted to understand these patterns of offspring desertion by using laboratory experiments to compare the fitness costs associated with parental care for each sex and the residual reproductive value of the 2 sexes. We also tested whether current brood size and residual reproductive value together predicted the incidence of brood desertion. We found that males and females each sustained fecundity costs as a consequence of caring for larvae and that these costs were of comparable magnitude. Nevertheless, males had greater residual reproductive value than females and were more likely than females to desert experimental broods. Our results can explain why males desert the brood earlier than females in nature and why female-only care is more common than male-only care. They also suggest that the tipping point from brood parasitism or satellite male behavior to communal breeding (and vice versa) depends on the value of the current brood relative to residual reproductive value.

Host–parasite relatedness shown by protein fingerprinting in a brood parasitic bird

Brood parasitism as an alternative female breeding tactic is particularly common in ducks, where hosts often receive eggs laid by parasitic females of the same species and raise their offspring. Herein, we test several aspects of a kin selection explanation for this phenomenon in goldeneye ducks (Bucephala clangula) by using techniques of egg albumen sampling and statistical bandsharing analysis based on resampling. We find that host and primary parasite are indeed often related, with mean r = 0.13, about as high as between first cousins. Relatedness to the host is higher in nests where a parasite lays several eggs than in those where she lays only one. Returning young females parasitize their birth nestmates (social mothers or sisters, which are usually also their genetic mothers and sisters) more often than expected by chance. Such adult relatives are also observed together in the field more often than expected and for longer periods than other females. Relatedness and kin discrimination, which can be achieved by recognition of birth nestmates, therefore play a role in these tactics and probably influence their success.

The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons

Hypothesis: In parasites that use hosts for offspring development, adults may base oviposition decisions on a range of host traits related either to host quality or the co-evolutionary relationship between parasite and host. We examined whether host quality or co-evolutionary dynamics drive the use of hosts in the bitterling-mussel relationship. Organisms: Six species of bitterling fish (Acheilognathinae) and eight species of freshwater mussels (Unionidae, Corbiculidae) that are used by bitterling for oviposition. Site of experiments: Experimental tanks in Wuhan, China, at the site of the natural distribution of the studied species. Methods: Three experiments that controlled for host accessibility and interspecific interactions were conducted to identify host preferences among bitterling fishes and their mussel hosts. We started with a broad interspecific comparison. We then tested bitterling behavioural choices, their temporal stability, and mussel host ejection behaviour of the eggs of generalist and specialist bitterling species. Finally, we measured host mussel quality based on respiration rate and used published studies on mussel gill structure to infer mussel suitability as hosts for bitterling eggs. Results: We found significant interspecific differences among bitterling species in their use of mussel hosts. Bitterling species varied in their level of host specificity and identity of preferred hosts. Host preferences were flexible even among apparently specialized species and fishes switched their preferences adaptively when the quality of individuals of preferred host species declined. Mussels varied considerably in their response to oviposition through egg ejections. Host preference by a generalist bitterling species correlated positively with host quality measured as the efficiency of the mussel gills to extract oxygen from inhaled water. Host ability to eject bitterling eggs correlated positively with their relative respiration rate, probably due to a higher velocity of water circulating in the mussel gill chamber.

The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe

Interspecific symbiotic relationships involve a complex network of interactions, and understanding their outcome requires quantification of the costs and benefits to both partners. We experimentally investigated the costs and benefits in the relationship between European bitterling fish (Rhodeus sericeus) and freshwater mussels that are used by R. sericeus for oviposition. This relationship has hitherto been thought mutualistic, on the premise that R. sericeus use mussels as foster parents of their embryos while mussels use R. sericeus as hosts for their larvae. We demonstrate that R. sericeus is a parasite of European mussels, because it (i) avoids the cost of infection by mussel larvae and (ii) imposes a direct cost on mussels. Our experiments also indicate a potential coevolutionary arms race between bitterling fishes and their mussel hosts; the outcome of this relationship may differ between Asia, the centre of distribution of bitterling fishes, and Europe where they have recently invaded.

Breeding Biology of Grassland Birds in Western New York: Conservation and Management Implications

Declining grassland breeding bird populations have led to increased efforts to assess habitat quality, typically by estimating density or relative abundance. Because some grassland habitats may function as ecological traps, a more appropriate metric for determining quality may be breeding success. Between 1994 and 2003 we gathered data on the nest fates of Eastern Meadowlarks (Sturnella magna), Bobolinks (Dolichonyx oryzivorous), and Savannah Sparrows (Passerculus sandwichensis) in a series of fallow fields and pastures/hayfields in western New York State. We calculated daily survival probabilities using the Mayfield method, and used the logistic-exposure method to model effects of predictor variables on nest success. Nest survival probabilities were 0.464 for Eastern Meadowlarks (n = 26), 0.483 for Bobolinks (n = 91), and 0.585 for Savannah Sparrows (n = 152). Fledge dates for first clutches ranged between 14 June and 23 July. Only one obligate grassland bird nest was parasitized by Brown-headed Cowbirds (Molothrus ater), for an overall brood parasitism rate of 0.004. Logistic-exposure models indicated that daily nest survival probabilities were higher in pastures/hayfields than in fallow fields. Our results, and those from other studies in the Northeast, suggest that properly managed cool season grassland habitats in the region may not act as ecological traps, and that obligate grassland birds in the region may have greater nest survival probabilities, and lower rates of Brown-headed Cowbird parasitism, than in many parts of the Midwest.

The Importance of Agriculture-Dominated Landscapes and Lack of Field Border Effect for Early-Succession Songbird Nest Success

In recent decades, many early-succession songbird species have experienced severe and widespread declines, which often are related to habitat destruction. Field borders create additional or enhance existing early-succession habitat on farmland. However, field border shape and the landscape context surrounding farms may influence the effectiveness of field borders in contributing to the stabilization or increase of early-succession bird populations. We examined the influence of linear and nonlinear field borders on farms in landscapes dominated by either agriculture or forests on nest success and Brown-headed Cowbird (Molothrus ater) brood parasitism of Indigo Bunting (Passerina cyanea) and Blue Grosbeak (Passerina caerulea) nests combined. Field border establishment did not affect nest survival probability and brood parasitism frequency of Indigo Bunting and Blue Grosbeak nests. Indigo Bunting/Blue Grosbeak nest success probability was more than twice as high in agriculture-dominated landscapes (39%) than in forested landscapes (17%), and brood parasitism frequency was high (33%) but did not differ between landscapes. Edges in agriculture-dominated landscapes can be higher-quality habitats for early-succession birds than edges in forest-dominated landscapes, but our field border treatments did not enhance nest success for these birds on farms in either landscape.

Morphology, molecular phylogeny, and taxonomic inconsistencies in the study of Bradypus sloths (Pilosa: Bradypodidae)

This study focuses on morphological and molecular data analyses, misidentifications, and phylogenetic inconsistencies regarding Bradypus variegatus (the brown-throated sloth) and B. tridactylus (the pale-throated sloth). Misidentifications were recorded on 75 of 313 museum specimens of Bradypus. Almost 90% of the misidentified specimens were B. variegatus from north-central Brazil, erroneously attributed to B. tridactylus. These misidentified specimens are reported in taxonomic reviews as the southernmost records of B. tridactylus. A history of confusing nomenclature regarding sloth species exists, and these particular misidentifications could be attributable to the similarity in face and throat color between B. variegatus from north-central Brazil and B. tridactylus. The molecular phylogeny of morphologically confirmed sloth specimens exhibits 2 monophyletic lineages representing B. variegatus and B. tridactylus. The split time between these 2 lineages was estimated at 6 million years ago (mya), contradicting previous studies that estimated this divergence to be 0.4 mya. Taxonomic inconsistencies were detected when comparing the molecular phylogeny to previously published DNA sequences ascribed to B. tridactylus. Misidentification or introgression could underlie such phylogenetic incongruities. Regardless of their causes, these discrepancies lead to misstatements regarding geographic distribution, phylogeny, and taxonomy of B. variegatus and B. tridactylus.

Análise filogenética e implicações sistemáticas e evolutivas nos Cuculiformes (Aves) com base na osteologia, comportamento e ecologia

Têm-se notado vários estudos recentes em filogenia com os Cuculiformes, no entanto nestes trabalhos ainda há divergências. Apresenta-se aqui uma nova e ampla análise filogenética para os Cuculiformes com base em 250 caracteres da osteologia, comportamento e ecologia. Esta análise resultou em 18 cladogramas igualmente parcimoniosos (768 passos, IC = 0.4779, IR = 0.8080 e ICR = 0.3861). de acordo com o cladograma de consenso estrito se pode observar: a) o monofiletismo dos Cuculiformes; b) a ordem dividida em dois grupos: a) Coua/Carpococcyx e; b) demais cucos (Neomorphidae, (Crotophagidae, (Tapera/Dromoccoccyx, (Cuculidae))), no entanto a posição sistemática de Centropus é ambígua entre estes dois grandes grupos; c) os cucos terrestres basais e parafiléticos e os cucos arbóreos derivados e monofiléticos. Ainda, propõe-se que o comportamento de parasitar ninho tenha surgido duas vezes independentemente (uma em Tapera/Dromoccoccyx e outra dentro de Cuculidae).

Analysis of genetic parentage in the tawny owl (Strix aluco) reveals extra-pair paternity is low

We have investigated genetic parentage in a Swiss population of tawny owls (Strix aluco). To this end, we performed genetic analysis for six polymorphic loci of 49 avian microsatellite loci tested for cross-species amplification. We found one extra-pair young out of 137 (0.7%) nestlings in 37 families (2.7%). There was no intra-specific brood parasitism. Our results are in accordance with previous findings for other raptors and owls that genetic monogamy is the rule. Female tawny owls cannot raise offspring without a substantial contribution by their mates. Hence one favoured hypothesis is that high paternal investment in reproduction selects for behaviour that prevents cuckoldry.

Nest predation by cowbirds and its consequences for passerine demography.

Brood parasitism by brown-headed cowbirds (Molothrus ater) reduces reproductive success in many passerines that nest in fragmented habitats and ecological edges, where nest predation is also common. We tested the hypothesis that parasitism and predation are often linked because cowbirds depredate nests discovered late in the host's nesting cycle to enhance future opportunities for parasitism. Over a 20-year study period, brood parasitism by cowbirds was a prerequisite to observing marked inter- and intraannual variation in the rate of nest failure in an insular song sparrow (Melospiza melodia) population. Nest failure increased with the arrival and laying rate of cowbirds and declined when cowbirds ceased laying. The absence or removal of cowbirds yielded the lowest nest failure rates recorded in the study. The absence of cowbirds also coincided with the absence of an otherwise strong positive correlation between host numbers and the annual rate of nest failure. Host numbers, cowbird parasitism, and nest failure may be correlated because cowbirds facilitate nest failure rather than cause it directly. However, an experiment mimicking egg ejection by cowbirds did not affect nest failure, and, contrary to the main prediction of the predation facilitation hypothesis, naturally parasitized nests failed less often than unparasitized nests. Higher survival of parasitized nests is expected under the cowbird predation hypothesis when female cowbirds defend access to hosts because cowbirds should often depredate unparasitized nests but should not depredate nests they have laid in. Where female cowbirds have overlapping laying areas, we expect parasitized nests to fail more often than others if different cowbirds often discover the same nests. We suggest that nest predation by cowbirds represents an adaptation for successful parasitism and that cowbirds influence host demography via nest predation.

Chic chicks: the evolution of chick ornamentation in rails

Competition over access to food has led to the evolution of a variety of exaggerated visual and vocal displays in altricial nestling birds. Precocial chicks that are fed by their parents also vary widely in appearance ranging from those with inconspicuous coloration to those with brightly colored bills, fleshy parts, and plumes. These ornaments are lost by the end of the period of parental dependence, suggesting they function in competition over parental care. We use a comparative approach to evaluate which ecological or life-history variables may have favored the evolution of conspicuous ornamentation in precocial chicks. We compiled data on chick morphology, ecology, and social organization of species in the Family Rallidae, a group with highly variable downy chicks. Chick ornamentation in the form of brightly colored bills, fleshy patches, or plumes is observed in 36 of 97 species for which downy chicks are described. Phylogenetic reconstructions suggest that nonornamentation is the ancestral state. Chick ornamentation has evolved multiple times within the Rallidae and is significantly associated with large clutch sizes and polygamous mating systems. Chick ornamentation was also weakly associated with adult ornamentation and adult dimorphism. We argue that these results support the hypothesis that lineages with higher levels of sibling competition are more likely to evolve ornamented chicks.

Reticence or vigilance at the nest: a cruel bind for the endangered Black-capped Vireo

Breeding birds vocalize to find mates and establish and defend territories, but these same critical communications may also attract predators or brood parasites, placing birds in a cruel bind. Although vigilant birds may better maintain social relationships with mates and neighbors through frequent vocalizations, reticent birds may reduce risk to their nests by being relatively quiet and making infrequent vocalizations. Selection for vocalization patterns that minimize brood parasitism might be particularly strong for birds that are unable to fledge both their own young and the parasite. Temporal plasticity in the frequency of vocalizations near nests, however, may allow birds to balance trade-offs and optimize nest-defense strategies. The Black-capped Vireo (Vireo atricapilla) is an endangered songbird that faces intensive brood parasitism in areas where Brown-headed Cowbirds (Molothrus ater) are present. Vireo nests that produce cowbird fledglings always fail to fledge vireo young. We recorded vocalizations at vireo nests across three nesting stages (building, laying, and early incubation) and three periods of the day (morning, midday, and evening) and compared vocalization frequency with eventual depredation or parasitism fate as well as local cowbird density to test two hypotheses. The predator-attraction hypothesis predicts that predators will be attracted by frequent vocalizations, whereas cowbirds will parasitize nests with relatively quiet parents and less predation risk; thus, vireos will experience trade-offs between reticence and vigilance in mediating specific risks. The parasite-assessment hypothesis predicts that vireos will become more secretive as local cowbird densities increase. Vireo vocalization response to nest predation and parasitism risk interacted with nest stage, and we found little evidence of risk mediation through vocalizations except during the building stage. Vireos, however, did benefit overall by optimizing temporal patterns in vocalizations. Vireo nests were less likely to be depredated or parasitized if males vocalized most during laying and least during the middle of the day. Birds vocalized more during the midday and less during the laying period when local cowbird densities were higher, however, perhaps demonstrating limited plasticity in social communication.