Edge effects reduce the nesting success of Acadian Flycatchers in a moderately fragmented forest

ABSTRACT.   Forest fragmentation can create negative edge effects that reduce the reproductive success of birds nesting near the forest/nonforest interface, and threaten bird populations deeper in remnant forest habitats. Negative edge effects may be more pronounced in landscapes that are moderately fragmented, particularly where agriculture is the primary land-use fragmenting forests. Information about the extent and strength of edge effects at a site can help guide conservation actions, and determine their effectiveness. We examined edge effects for birds breeding in a nearly contiguous forest fragmented by relatively narrow agricultural corridors in Illinois (USA). We measured rates of nest predation and brood parasitism for Acadian Flycatchers ( Empidonax virescens ) over a continuum of distances from the edge of an agricultural inholding. Nest predation and brood parasitism were highest near the edge and decreased with increasing distance from the edge. Given the cumulative effects of nest predation and brood parasitism on reproductive success, we determined that forest within 600 m of the inholding was sink habitat. We found, however, that deeper forest interior areas currently serve as source habitat, and that conversion of the entire 205 ha agricultural corridor to forest would add 1350 ha of source habitat for Acadian Flycatchers. Such results provide support for a local conservation strategy of forest consolidation and establish baseline measures necessary to determine the relative effectiveness of any subsequent reforestation efforts.     

Nest destruction elicits indiscriminate con‐ versus heterospecific brood parasitism in a captive bird

Following nest destruction, the laying of physiologically committed eggs (eggs that are ovulated, yolked, and making their way through the oviduct) in the nests of other birds is considered a viable pathway for the evolution of obligate interspecific brood parasitism. While intraspecific brood parasitism in response to nest predation has been experimentally demonstrated, this pathway has yet to be evaluated in an interspecific context. We studied patterns of egg laying following experimental nest destruction in captive zebra finches, Taeniopygia guttata, a frequent intraspecific brood parasite. We found that zebra finches laid physiologically committed eggs indiscriminately between nests containing conspecific eggs and nests containing heterospecific eggs (of Bengalese finches, Lonchura striata vars. domestica), despite the con‐ and heterospecific eggs differing in both size and coloration. This is the first experimental evidence that nest destruction may provide a pathway for the evolution of interspecific brood parasitism in birds.     

On the origin of brood parasitism in altricial birds

The probability that obligate interspecific brood parasitism(OP), among altricial birds evolved directly from the normalbreeding (no parasitism, NP) mode or indirectly through intraspecificnest parasitism (INP) was examined by using maximum-likelihoodand parsimony approaches. We examined the probability of ancestralstates at 24 key nodes in order to test our hypotheses. Thestate of the most basal node in a tree of 565 genera of altricialbirds is equivocal; however, the state probability of NP atthis node is about 5.5-fold more likely than the state of obligateparasite. A similar trend was observed for basal nodes of mostfamilies examined. The INP state was supported only in the Hirundinidae.The high incidence of INP among martins and swallows explainsthis finding. Contrary to our predictions, even in other groupswhere there is a high incidence of INP and OP, such as in thetribe Icteri and the Old World finches, the probability of NPbeing ancestral was very high. We conclude that in all casesbut one (Hirundinidae) obligate, and probably facultative, broodparasitism evolved directly from normal breeding mode ratherthan indirectly through some other form of parasitism.     

Experimental support for the role of nest predation in the evolution of brood parasitism

In 1965, Hamilton and Orians (HO) hypothesized that the starting point for the evolution of obligate interspecific brood parasitism in birds was the facultative laying of physiologically committed eggs in neighbouring active nests of con‐ and heterospecifics, following predation of a bird’s own nest during the laying stage. We tested this prediction of the HO hypothesis by using captive pairs of zebra finches (Taeniopygia guttata), a species with evidence for intraspecific parasitism both in the wild and in captivity. As predicted, in response to experimental nest removal, subjects laid eggs parasitically in simulated active conspecific nests above chance levels. Across subsequent trials, we detected both repeatability and directional change in laying patterns, with some subjects switching from parasitism to depositing eggs in the empty nest. Taken together, these results support the assumptions and predictions of the HO hypothesis, and indicate that the zebra finch is a potential model species for future behavioural and genetic studies in captive brood parasite research.     

Egg ejection cost can limit defence strategies against brood parasitism

A cost associated with the evolution of antiparasite strategies is the failure to recognize parasitic eggs, leading the host to evict its own eggs. However, there is evidence that birds recognize their own eggs through imprinting. This leads to the question of why birds accept parasitic eggs if such eggs can be identified. Here, we tested whether egg ejection per se can be costly due to increased predation risk to the remaining clutch and whether olfactory or visual cues of egg ejection increase predation. We carried out three field experiments to answer the following questions: (a) Does ejecting an egg increase nest predation risk? (b) Does the presence of olfactory cues, such as the smell of a broken egg, increase nest predation risk? And (c) Does the presence of visual cues, such as an egg shell below the nest, increase nest predation risk? We found evidence that egg ejection increases nest predation and that olfactory cues alone also increase nest predation. The presence of visual cues did not change predation rates. These data indicate that egg ejection is costly for both host and parasitic eggs that may remain in the nest. Our results suggest why host and parasite eggs are commonly found within the same nests, despite the possibility that hosts recognize and could possibly eject the parasite’s egg.     

鸟类巢寄生伤害理论的进化

鸟类巢寄生的寄主无论是成乌还是雏鸟,对宿主都是极具伤害性的,因为它们降低了宿主的生育力,然而,无论是在寄主种内还是种间,其伤害性的差异变化很大。综述了以往对这种伤害性差异的各种解释,以往的解释在很大程度上集中在伤害性所带来的利益。认为寄主的伤害性行为可以像病原体的伤害性一样进行分类,伤害性在为寄主带来利益的同时,也伴随着代价,所以,由病原体伤害性进化研究衍生而来的平衡假说,适用于解释鸟类巢寄生伤害理论的进化。     

The evolution of obligate interspecific brood parasitism in birds

We present a simple analytical model to investigate the conditionsfor the evolution of obligate interspecific brood parasitismin birds, based on clutch size optimization, when birds canlay more eggs than their optimal clutch size. The results showthat once intraspecific parasitism has appeared (i.e., femalesstart to spread their eggs over their own and other nests) the evolutionarily stable number of eggs laid in its own nest decreases.Two possible ESSs exist: (1) either the evolutionarily stablenumber of eggs laid in its own nest is larger than zero, anda fraction of the total number of eggs is laid parasitically(i.e., intraspecific parasitism); and (2) either the evolutionarilystable number of eggs laid in its own nest is zero and all eggs are laid parasitically. Since all females lay parasitically,this could favor the evolution of obligate interspecific broodparasitism. The key parameter allowing the shift from intraspecificto obligate interspecific parasitism is the intensity of density-dependentmortality within broods (i.e., nestling competition). Strongnestling competition, as in altricial species, can lead toan ESS where all eggs are laid parasitically. Altricial speciesare, therefore, predicted to evolve more easily toward obligate interspecific parasitism than precocial species. These predictionsfit the observed distribution of brood parasitism in birds,where only one species out of 95 obligate interspecific parasitesexhibits a precocial mode of development. Different nestlingsurvival functions provided similar findings (i.e., obligatebrood parasitism is more likely to evolve in altricial species),suggesting that these results are robust with respect to themain assumption of the model.     

Modelling the arms race in avian brood parasitism

In brood parasitism, interactions between a parasite and its host lead to a co-evolutionary process called an arms race, in which evolutionary progress on one side provokes a further response on the other side. The host evolves defensive means to reduce the impact of parasitism, while the parasite evolves means to counter the host's defence. To gain insights into the co-evolutionary process of the arms race, a model is developed and analysed, in which the host's defence and the parasite's counterdefence are assumed to be genetically determined. First, the effect of parasite counterdefence on host defence is analysed. I show that parasite counterdefence can critically affect the establishment of host defence, giving rise to three situations in the equilibrium state: The host shows (1) no defence, (2) an intermediate level of defence or (3) perfect defence. Based on these results, the evolution of parasite counterdefence is considered in connection with host defence. It is suggested that the parasite can evolve counterdefence to a certain degree, but once it has established counterdefence beyond this, the host gives up its defence against parasitism provided the defence entails some cost to perform. Dynamic aspects of selection pressure are crucial for these results. Based on these results, I propose a hypothetical evolutionary sequence in the arms race, along which interactions between the host and parasite proceed.     

Fluctuation of body temperature and cuckoo brood parasitism

Body temperatures of 11 bird species, including cuckoos, were measured in an artificial meteorological room. Ratios of change in body temperature to that in air temperature were thereby obtained for each species. Cuckoos demonstrate a remarkably high value, indicating a particularly low ability to regulate body temperature. Viewed in this light, the cuckoo's parasitic behavior is very likely an adaptation to overcome a physiological disadvantage. This in turn might be expected to reinforce delay in evolution of temperature homeostasis.     

The role of reed management and habitat quality on brood parasitism and chick survival of the brood parasitic Common Cuckoo

Despite efforts on ecosystem restoration and management, biodiversity loss remains one of the major environmental concerns of our time. Beyond the focus on threatened species, animals that indicate regional biodiversity hotspots and population trends, such as brood parasites, should also be targeted by conservation actions. We studied how reed habitat quality and management influence brood parasitism rate and offspring survival in Common Cuckoos Cuculus canorus parasitizing nests of Great Reed Warblers Acrocephalus arundinaceus in six reed habitats in an intensive agricultural landscape. Data collected from 45 sites over 13 years showed that the brood parasitism rate was highest on large canals and was positively influenced by the availability of potential perches (Cuckoo vantage points) and the height where host nests were built. Cuckoo chick survival decreased with water depth and was not affected by other factors. Our results suggest that the habitat-dependent detectability of host nests was central in brood parasitism rate and that water level was central in Cuckoo chick survival. Our study shows that a maintenance of intermediate water levels is the most optimal for maintaining Cuckoo populations in intensive agricultural landscapes. Because brood parasites are excellent bioindicators as their presence predicts regional hotspots of taxonomic and functional diversity as well as population trends in bird communities, knowledge on their habitat requirements is relevant in management targeting diverse bird communities.     

Distance from riparian edge reduces brood parasitism of southwestern willow flycatchers,whereas parasitism increases nest predation risk

The southwestern willow flycatcher (Empidonax traillii extimus) is a federally endangered subspecies that breeds in increasingly fragmented and threatened habitat. We examined whether temporal and habitat characteristics were associated with risk of predation and probability of brood parasitism by brown-headed cowbirds (Molothrus ater) on flycatcher nests at 6 sites in southern Nevada and northwestern Arizona, USA. For nest predation, we found the most support for a model that included date and an interaction between parasitism status and nesting stage. Daily nest survival decreased from 0.87 (95% CI = 0.81–0.93) to 0.78 (95% CI = 0.72–0.84) through the season for parasitized nests but remained relatively constant for unparasitized nests (0.93, 95% CI = 0.91–0.95 to 0.92, 95% CI = 0.91–93). Parasitized nests had lower survival than non-parasitized nests during the incubation (0.85, 95% CI = 0.84–0.86 vs. 0.92, CI = 0.91–0.93) and nestling (0.79, 95% CI = 0.77–0.81 vs. 0.91, 95% CI = 0.90–0.92) stages. Of the variables included in our parasitism candidate models, model-averaged coefficients and odds ratios supported only distance to habitat edge; odds of parasitism decreased 1% for every 1 m from the habitat edge. Nests greater than 100 m from an edge were 50% less likely to be parasitized as those on an edge, however, only 52 of 233 nests (22%) were found at this distance. Where management and conservation goals include reducing nest losses due to parasitism, we recommend restoration of habitat patches that minimize edge and maximize breeding habitat further from edges. At sites where cowbirds have been documented as important nest predators, controlling cowbirds may be one option, but further study of the link between parasitism and nest predation and the identification of major nest predators at specific sites is warranted. © 2011 The Wildlife Society.     

Individual patterns of habitat and nest-site use by hosts promote transgenerational transmission of avian brood parasitism status

Brood parasitic birds impose variable fitness costs upon their hosts by causing the partial or complete loss of the hosts' own brood. Growing evidence from multiple avian host-parasite taxa indicates that exposure of individual hosts to parasitism is not necessarily random and varies with habitat use, nest-site selection, age or other phenotypic attributes. For instance, nonrandom patterns of brood parasitism had similar evolutionary consequences to those of limited horizontal transmission of parasites and pathogens across space and time and altered the dynamics of both population productivity and co-evolutionary interactions of hosts and parasites. We report that brood parasitism status of hosts of brown-headed cowbirds Molothrus ater is also transmitted across generations in individually colour-banded female prothonotary warblers Protonotaria citrea. Warbler daughters were more likely to share their mothers' parasitism status when showing natal philopatry at the scale of habitat patch. Females never bred in their natal nestboxes but daughters of parasitized mothers had shorter natal dispersal distances than daughters of nonparasitized mothers. Daughters of parasitized mothers were more likely to use nestboxes that had been parasitized by cowbirds in both the previous and current years. Although difficult to document in avian systems, different propensities of vertical transmission of parasitism status within host lineages will have critical implications both for the evolution of parasite tolerance in hosts and, if found to be mediated by lineages of parasites themselves, for the difference in virulence between such extremes as the nestmate-tolerant and nestmate-eliminator strategies of different avian brood parasite species.     

A game theoretical approach to conspecific brood parasitism

We constructed a game theoretical model to predict optimal patternsof egg laying in systems where individuals lay in the nestsof others as well as in their own nests. We show that decreasingthe effect of position within an egg-laying sequence on theworth of an egg should lead to reduced parasitism. Indeed,parasitism can only flourish if the worth of an egg to its biological parent declines with the total number of eggs laid in that nest.Further, we found that increasing the intrinsic costs of eggproduction should lead to an increased propensity for conspecificbrood parasitism. The model also predicts that variation inhosts' ability to reject parasitic eggs has little effect on parasitism until this ability is well developed.     

Importance of spatial habitat structure on establishment of host defenses against brood parasitism

We used metapopulation dynamics to develop a mathematical simulationmodel for brood parasites and their hosts in order to investigatethe validity of the "spatial habitat structure hypothesis,"which states that a low level of parasite egg rejection in hostpopulations is due to the immigration of acceptor individualsfrom nonparasitized populations. In our model, we varied dispersalrate and the relative carrying capacity of host individualsin parasitized and unparasitized patches. When both the relativecarrying capacity in the parasite-free patch and the dispersalrate increase, the nonparasitized patch will provide more acceptorindividuals to the parasite-prone patch. As the relative carryingcapacity in the parasite-free patch increases, the equilibriumfrequency of rejecters both in the parasite-prone and in theparasite-free patch decreases toward zero for intermediate levelsof the dispersal rate. Although the rejecter strategy is moreadaptive than the acceptor strategy in the parasite-prone patch,large numbers of acceptors are produced in the parasite-freepatch dispersing to the parasitized patch. As the number ofindividuals in the parasite-free patch increases, parasitismrate can be maintained stable at a high equilibrium level inthe parasite-prone patch.     

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.     

Diet specialization and brood parasitism in cuckoo species

1. Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.
2. In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.
3. After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.
4. The findings of this study provide an additional understanding of the cuckoos’ ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

     

Host defense in Nicrophorus quadripunctatus against brood parasitism by Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae)

Few studies have been conducted on the host defenses of insects against brood parasitism. We investigated whether the silphid beetle Ptomascopus morio, a brood parasite of related silphid species Nicrophorus concolor, can also parasitize another silphid species Nicrophorus quadripunctatus and the manner in which N. quadripunctatus defends itself against parasitism. Successful brood parasitism under natural conditions was not observed at the time of year when P. morio and N. quadripunctatus are both reproductively active. Follow-up experiments revealed that P. morio attempts to oviposit near N. quadripunctatus nests, but is rarely successful if adult hosts are present. When P. morio larvae were experimentally introduced to N. quadripunctatus broods, some P. morio larvae survived when the host and parasite larvae were at the same stage. We concluded that N. quadripunctatus defends itself against brood parasitism in two ways: (1) potential brood parasites are repelled, thus limiting their access to the resource; and (2) the young of the parasitic species are killed.     

Molecular phylogeny of cuckoos supports a polyphyletic origin of brood parasitism

We constructed a molecular phylogeny of 15 species of cuckoos using mitochondrial DNA sequences spanning 553 nucleotide bases of the cytochrome b gene and 298 nucleotide bases of the ND2 gene. A parallel analysis for the cytochrome b gene including published sequences in the Genbank database was performed. Phylogenetic analyses of the sequences were done using parsimony, a sequence distance method (Fitch-Margoliash), and a character-state method which uses probabilities (maximum likelihood). Phenograms support the monophyly of three major clades: Cuculinae, Phaenicophaeinae and Neomorphinae-Crotophaginae. Clamator, a strictly parasitic genus traditionally included within the Cuculinae, groups together with Coccyzus (a nonobligate parasite) and some nesting cuckoos. Tapera and Dromococcyx, the parasitic cuckoos from the New World, appear as sister genera, close to New World cuckoos: Neomorphinae and Crotophaginae. Based on the results, and being conscious that a more strict resolution of the relationships among the three major clades is required, we postulate that brood parasitism has a polyphyletic origin in the Cuculiformes, with parasite species being found within the three defined clades. Evidence suggests that species within each clade share a common parasitic ancestor, but some show partial or total loss of brood parasitic behaviour.     

Interspecific brood parasitism in galliform birds

Mode of development in birds helps determine the form of brood parasitism a species exhibits. Most knowledge of precocial brood parasites comes from a single avian family, the waterfowl (Anatidae: Anseriformes). Here we review cases of interspecific brood parasitism (IBP) in a second group of precocial birds, the order Galliformes. IBP is uncommon but taxonomically widespread, occurring in at least 11 species and in four of five galliform families. By far the most common brood parasite is the Ring-necked Pheasant Phasianus colchicus . Hosts were generally other ground-nesting precocial species. It is unclear whether the absence of IBP in the Cracidae (Guans, Curassows, and Chachalacas) is due to the paucity of research on tropical gamebirds or because tropical birds such as the Cracidae may be less likely to practise IBP. Galliform birds mirror the trend found in ducks in which virtually all species that parasitize heterospecifics are also conspecific brood parasites (CBP). This association supports the hypothesis that IBP as an adaptive tactic or strategy may evolve from CBP. Alternatively, or additionally, egg-dumping may represent reproductive error on the part of females, such that concordance between CBP and IBP could be a byproduct of having sufficient knowledge of breeding biology only for a subset of galliform species.     

Inter‐specific brood parasitism and the evolution of avian reproductive strategies

Avian brood parasitism is a potent selective agent modulating host behaviors and morphology, although its role in determining diversification of avian breeding strategies remains elusive. Hitherto, the study of selection of brood parasites on host breeding strategies has been based on single reproductive trait approaches, which neglect that evolutionary responses to brood parasites may involve co‐ordinated changes in several aspects of reproduction. Here I consider covariation among reproductive traits to test whether parental breeding strategies of hosts of brown headed cowbird (BHC hereafter) in North America and the common cuckoo (CC hereafter) in Europe, two parasites with contrasting level of virulence, have evolved in response to brood parasitism. The effect of parasitism on avian breeding strategies differed between continents. Long term exposure to BHC parasitism selected for a lower breeding investment in North America, but not so CC parasitism in Europe. These results suggest a key role of parasite virulence on the evolution of avian breeding strategies and that brood parasitism has selected for a co‐ordinated breeding strategy of reducing parasitism costs by shortening and fractioning reproductive events within a single season in North America.