Parental care in the Small Tree Finch Camarhynchus parvulus in relation to parasitism and environmental factors

The parental food compensation hypothesis suggests that parents may compensate for the negative effects of parasites on chicks by increased food provisioning. However, this ability differs widely among host species and may also depend on ecological factors such as adverse weather conditions and habitat quality. Although weed management can improve habitat quality, management measures can bring about a temporary decrease in food availability and thus may reduce parents’ ability to provide their nestlings with enough energy. In our study we investigated the interaction of parasitism and weed management, and the influence of climate on feeding rates in a Darwin’s tree finch species, which is negatively impacted by two invasive species. The larvae of the invasive parasitic fly Philornis downsi ingest the blood and body tissues of tree finch nestlings, and the invasive Blackberry Rubus niveus affects one of the main habitats of Darwin’s tree finches. We compared parental food provisioning of the Small Tree Finch Camarhynchus parvulus in parasitized and parasite‐free nests in three different areas, which differed in invasive weed management (no management, short‐term and long‐term management). In a parasite reduction experiment, we investigated whether the Small Tree Finch increases food provisioning rates to nestlings when parasitized and whether this ability depends on weed management conditions and precipitation. Our results provide no evidence that Small Tree Finches can compensate with additional food provisioning when parasitized with P. downsi. However, we found an increase in male effort in the short‐term management area, which might indicate that males compensate for lower food quality with increased provisioning effort. Furthermore, parental food provisioning was lower during rainfall, which provides an explanation for the negative influence of rain on breeding success found in earlier studies. Like other Darwin’s finches, the Small Tree Finch seems to lack the ability to compensate for the negative effects of P. downsi parasitism, which is one explanation for why this invasive parasite has such a devastating effect on this host species.     

Host‐specific associations affect the microbiome of Philornis downsi,an introduced parasite to the Galápagos Islands

The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host–parasite co‐evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host‐related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.     

Experimental demonstration of the fitness consequences of an introduced parasite of Darwin's finches

Background

Introduced parasites are a particular threat to small populations of hosts living on islands because extinction can occur before hosts have a chance to evolve effective defenses. An experimental approach in which parasite abundance is manipulated in the field can be the most informative means of assessing a parasite''s impact on the host. The parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, feeds on nestling Darwin''s finches and other land birds. Several correlational studies, and one experimental study of mixed species over several years, reported that the flies reduce host fitness. Here we report the results of a larger scale experimental study of a single species at a single site over a single breeding season.

Methodology/Principal Findings

We manipulated the abundance of flies in the nests of medium ground finches (Geospiza fortis) and quantified the impact of the parasites on nestling growth and fledging success. We used nylon nest liners to reduce the number of parasites in 24 nests, leaving another 24 nests as controls. A significant reduction in mean parasite abundance led to a significant increase in the number of nests that successfully fledged young. Nestlings in parasite-reduced nests also tended to be larger prior to fledging.

Conclusions/Significance

Our results confirm that P. downsi has significant negative effects on the fitness of medium ground finches, and they may pose a serious threat to other species of Darwin''s finches. These data can help in the design of management plans for controlling P. downsi in Darwin''s finch breeding populations.     

Effects of the introduced ectoparasite Philornis downsi on haemoglobin level and nestling survival in Darwin's Small Ground Finch (Geospiza fuliginosa)

Abstract: The physiological impacts and fitness costs of parasitism by an introduced ectoparasitic fly, Philornis downsi (Muscidae), were studied in nestlings of Darwin's Small Ground Finch, Geospiza fuliginosa (Geospizinae), on the Galápagos Archipelago. Whole blood haemoglobin (Hb) concentration was used to measure host response to ectoparasitism due to its high repeatability and validity, as well as for its key role in aerobic activities that affect fitness, such as flight capacity and nestling begging intensity. Increased numbers of ectoparasitic larvae of P. downsi were strongly correlated with lower Hb levels in nestlings in the absence of blood parasites. Furthermore, immature red blood cell counts were negatively correlated with Hb level and positively correlated with P. downsi intensity. Nestlings with high levels of parasitism suffered higher mortality, which varied with clutch size. Our results provide evidence that endemic Galápagos bird populations are physiologically compromised by P. downsi and experience substantial fitness costs due to ectoparasitism.     

Behavior of the Avian Parasite Philornis downsi (Diptera: Muscidae) in and Near Host Nests in the Galapagos Islands

The Avian Vampire Fly, Philornis downsi, has invaded the Galapagos Islands, where it causes high mortality of endemic and native landbird species, including most species of Darwin’s finches. Control methods are under development, but key information is missing about the reproductive biology of P. downsi and the behavior of flies in and near nests of their hosts. We used external and internal nest cameras to record the behavior of P. downsi adults within and outside nests of the Galapagos Flycatcher, Myiarchus magnirostris, throughout all stages of the nesting cycle. These recordings showed that P. downsi visited flycatcher nests throughout the day with higher fly activity during the nestling phase during vespertine hours. The observations also revealed that multiple P. downsi individuals can visit nests concurrently, and that there are some interactions among these flies within the nest. Fly visitation to nests occurred significantly more often while parent birds were away from the nest than in the nest, and this timing appears to be a strategy to avoid predation by parent birds. We report fly mating behavior outside the nest but not in the nest cavity. We discuss the relevance of these findings for the adaptive forces shaping P. downsi life history strategies as well as rearing and control measures.

     

Under adverse conditions,older small tree finch males (Camarhynchus parvulus) produce more offspring than younger males

Females of many bird species prefer mating with older males, presumably because they provide superior parental care and possibly superior genes. A previous study found that female small tree finches (Camarhynchus parvulus) preferred pairing with old males and had a higher breeding success when paired with old males because their nests were more concealed, higher up in the canopy and therefore less likely to be depredated. However, causes for brood loss have changed over the last decade: predation of small tree finch nests has decreased, whereas brood losses due to parasitism by the invasive parasitic fly Philornis downsi have increased. In the present study, we investigated (a) how the change in predation and parasitism by P. downsi influenced the breeding success of small tree finches, (b) whether there were still differences in breeding success between young and old males, (c) whether P. downsi infestation had a differential effect on nests of young and old males and (d) whether young and old males differed in foraging success. During 2012–2016, we found an overall low influence of predation and a high influence of P. downsi, but neither differed between nests of young and old males. Nests of old males had more fledglings than those of young males. However, the difference in breeding success disappeared when P. downsi numbers were experimentally reduced by injecting an insecticide into nests. This indicates that older males were able to compensate for the detrimental effects of parasitism.     

Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper)

Darwin’s medium tree finch (Camarhynchus pauper) meets the 2009 International Union for Conservation of Nature Red List criteria for a critically endangered species because it has “a very small range on a single island” and is “declining rapidly owing to the effects of the parasite Philornis downsi”, habitat degradation, and introduced predators. The medium tree finch is only found in patches of remnant highland forest on Floreana Island, where it co-exists with breeding populations of small and large tree finches (C. parvulus and C. psittacula). Here, we examine the intensity of P. downsi in nests of small, medium, and large tree finches on Floreana. We expected that parasite intensity would increase with finch body size, and with greater rainfall, and would also correlate with increased nestling mortality. We found a trend in the expected direction for parasite intensity and rainfall. Combined meta-analytically with data from a previous study, the overall trend for the two studies was significant. We also found a significant linear trend in parasite intensity with finch body size. In addition, the medium tree finch exhibited a somewhat higher parasite intensity than would be expected based on body mass alone. Of 63 active medium tree finch nests, 17 nests had nestlings: all of which were infested with P. downsi. Only 25% of medium tree finch nestlings fledged, 28% were depredated, 41% died due to P. downsi parasitism, and 6% died for other reasons.     

Ecoimmunity in Darwin's Finches: Invasive Parasites Trigger Acquired Immunity in the Medium Ground Finch (Geospiza fortis)

Background

Invasive parasites are a major threat to island populations of animals. Darwin''s finches of the Galápagos Islands are under attack by introduced pox virus (Poxvirus avium) and nest flies (Philornis downsi). We developed assays for parasite-specific antibody responses in Darwin''s finches (Geospiza fortis), to test for relationships between adaptive immune responses to novel parasites and spatial-temporal variation in the occurrence of parasite pressure among G. fortis populations.

Methodology/Principal Findings

We developed enzyme-linked immunosorbent assays (ELISAs) for the presence of antibodies in the serum of Darwin''s finches specific to pox virus or Philornis proteins. We compared antibody levels between bird populations with and without evidence of pox infection (visible lesions), and among birds sampled before nesting (prior to nest-fly exposure) versus during nesting (with fly exposure). Birds from the Pox-positive population had higher levels of pox-binding antibodies. Philornis-binding antibody levels were higher in birds sampled during nesting. Female birds, which occupy the nest, had higher Philornis-binding antibody levels than males. The study was limited by an inability to confirm pox exposure independent of obvious lesions. However, the lasting effects of pox infection (e.g., scarring and lost digits) were expected to be reliable indicators of prior pox infection.

Conclusions/Significance

This is the first demonstration, to our knowledge, of parasite-specific antibody responses to multiple classes of parasites in a wild population of birds. Darwin''s finches initiated acquired immune responses to novel parasites. Our study has vital implications for invasion biology and ecological immunology. The adaptive immune response of Darwin''s finches may help combat the negative effects of parasitism. Alternatively, the physiological cost of mounting such a response could outweigh any benefits, accelerating population decline. Tests of the fitness implications of parasite-specific immune responses in Darwin''s finches are urgently needed.     

Host tolerance and resistance to parasitic nest flies differs between two wild bird species

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Low survival of parasite chicks may result from their imperfect adaptation to hosts rather than expression of defenses against parasitism

Host parents exhibit a variety of behaviors toward avian brood parasites, but not all of their actions have necessarily evolved in response to costs imposed by parasites. To investigate whether common waxbills (Estrilda astrild) have evolved defenses specifically against parasitic pin-tailed whydahs (Vidua macroura), I studied the specificity and flexibility of host behaviors toward nestlings at two sites that differed significantly in parasitism rates and intensities. I focused on documenting nestling survival because V. macroura young match the elaborate gape morphology of E. astrild nestlings, a pattern that suggests hosts may possess unique defenses against parasite chicks. Parasite young survived significantly worse than host young in mixed broods. However, this apparent discrimination was not associated with parasitism risk as would be expected if defenses had evolved specifically to counter parasitism. Parasite young may have survived poorly compared to host young because individual chicks were less able to stimulate sufficient care from foster parents or because they were more susceptible to nestling competition, disease, or reduced provisioning by hosts. Mortality may have also been exacerbated by poor timing of parasite egg laying. In nonparasitized and parasitized nests, rates of nestling survival were similar, further suggesting that parenting behaviors that result in chick mortality did not evolve solely in response to parasite young. In addition, orange-breasted waxbills (Amandava subflava) and zebra finches (Taeniopygia guttata), rarely parasitized and nonparasitized relatives of E. astrild, experience similar levels of nestling mortality presumably as a result of phylogenetically widespread parenting strategies. Despite the similarity of parasitic V. macroura nestlings and E. astrild nestlings, I found no evidence that E. astrild parents possess defenses that allow for specific discrimination against parasite chicks during the nestling period. Rather than being subject to host defenses evolved in an arms race, Vidua chicks may simply be imperfectly adapted to life in the nests of their hosts.     

Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin’s finches

Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade‐offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The ‘fecundity advantage hypothesis’ predicts female‐biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis‐causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in‐nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12‐year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host–parasite system.     

Offspring survival is negatively related to maternal response to sheep red blood cells in zebra finches

The immune system is an important player in individual trade-offs, but what has rarely been explored is how different strategies of investment in immune response may affect reproductive decisions. We examined the relationship between the strength of maternal immune response and offspring viability and immune response in captive zebra finches Taeniopygia guttata. In three independent experiments, the females and subsequently their adult offspring were challenged with sheep red blood cells, and their responses were measured. There was no relationship between offspring immune response and that of their mothers. However, we found offspring survival until adulthood to be negatively related to maternal antibody titers. That effect was consistent among all experiments and apparent despite the fact that we partially cross-fostered newly hatched nestlings between nests of different females. This suggests that the observed effects of maternal immune response is not mediated by potentially altered female rearing abilities. To our knowledge, this is the first study showing the relationship between the strength of the immune response and between-generational fitness costs in birds.     

Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict?

Parent-offspring conflict may arise because the lifetime reproductive success of the parent is more influenced by its life span than by reproductive success during a particular reproductive event, while the fitness of an offspring depends firstly on its own survival as a juvenile and only subsequently on its own reproductive success. The naive immune system of young animals may allow offspring to be much more affected by parasites than their parents, and thus cause an initial asymmetry in a potential parent-offspring conflict. We investigated this type of conflict by assessing the health status and the immune response of parent and offspring sand martins Riparia riparia infested with manipulated loads of ticks Ixodes lividus (nests either treated with pyrethrin, water, or just visited). The prevalence and the intensity of tick infestations differed among treatments, with low tick loads in nests with the pyrethrin treatment. Ticks reduced the reproductive success of the host and increased offspring wing length. Broods with ticks had higher leukocyte concentrations and concentrations of immunoglobulins. The concentration of immunoglobulins in nestlings was negatively related to brood size and nestling tarsus length. Nestlings receiving the control treatments had a positive association between wing length and the concentration of immunoglobulins and a negative association between tarsus length and immunoglobulins. In contrast, adult sand martins did not respond to the parasite treatment in terms of immune response. Hence, the naive immune system of nestlings may be the crucial factor causing the parent-offspring conflict over costs of parasitism to be resolved to the advantage of parents that may sacrifice nestlings in heavily parasitized nests. Received: 30 March 1998 / Accepted: 5 December 1998     

Nest‐dwelling ectoparasites reduce begging effort in Pied Flycatcher Ficedula hypoleuca nestlings

Parasitized nestlings might be expected to increase begging effort to obtain additional resources to compensate for those sequestered by their parasites. However, begging is costly and chicks harbouring parasites may find it more difficult to attain high begging levels. Consequently, we predicted that, for the same level of nutritional need, nestlings that are parasitized will invest less in begging than those that are not parasitized. We tested this prediction by measuring begging in Pied Flycatcher Ficedula hypoleuca nestlings parasitized with haematophagous mites Dermanyssus gallinoides and Dermanyssus gallinae and blowfly larvae Protocalliphora azurea, and subjected to different levels of food deprivation in order to control for short‐term nutritional need. Nestlings from nests with ectoparasites spent less time begging than those from nests without parasites, especially when very hungry, although there was no association with latency to beg or begging intensity. Our results suggest that time invested in begging may indicate not only the level of need, but also nestling parasitism status.     

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum‐likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host‐associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall‐forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host‐plant‐associated differentiation were greater in the non‐gall‐inducing parasites than in their gall‐inducing hosts. RNA‐seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host‐plant relationships. Our results suggest a mode of speciation in which host plants drive within‐guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.     

Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (<Emphasis Type="Italic">Philornis downsi</Emphasis>) of Galápagos birds

The natural reproductive behaviour of invasive insects is pivotal knowledge for managing species of ecological or economic concern. We use microsatellites to examine female multiple mating and multiple nest infestations in the introduced parasitic fly, Philornis downsi, which causes high mortality in endemic birds on the Galápagos Islands. We analyse larvae and pupae within 57 nests from Santa Cruz and Floreana Islands in both the highland and lowland habitats. Sib-ship reconstructions of offspring revealed that up to five females may infest a single nest, while multiple mating in females was frequent (65% of reconstructed maternal genotypes), with an average of 1.91 (±0.06 SE) males per female. Genetic relatedness (R) of offspring within nests was generally low, though lowland nests on Floreana had higher R than highland nests. Knowledge of the reproductive behaviour of P. downsi is necessary for modelling appropriate management strategies, in particular, the sterile insect technique, for which success is greatly influenced by female multiple mating.     

Apparent vector‐mediated parent‐to‐offspring transmission in an avian malaria‐like parasite

Parasite transmission strategies strongly impact host–parasite co‐evolution and virulence. However, studies of vector‐borne parasites such as avian malaria have neglected the potential effects of host relatedness on the exchange of parasites. To test whether extended parental care in the presence of vectors increases the probability of transmission from parents to offspring, we used high‐throughput sequencing to develop microsatellites for malaria‐like Leucocytozoon parasites of a wild raptor population. We show that host siblings carry genetically more similar parasites than unrelated chicks both within and across years. Moreover, chicks of mothers of the same plumage morph carried more similar parasites than nestlings whose mothers were of different morphs, consistent with matrilineal transmission of morph‐specific parasite strains. Ours is the first evidence of an association between host relatedness and parasite genetic similarity, consistent with vector‐mediated parent‐to‐offspring transmission. The conditions for such ‘quasi‐vertical’ transmission may be common and could suppress the evolution of pathogen virulence.     

Sheep in wolf's clothing: host nestling vocalizations resemble their cowbird competitor's

Nestlings of many avian brood parasites are virtuosos at mimicking host nestling vocalizations, which, like egg mimicry, presumably ensures acceptance by host parents. Having been accepted, parasitic nestlings then often exaggerate the aspects of the host's display to increase parental care. Host nestlings may, in turn, exaggerate their vocalizations to keep up with the parasite, though this possibility has not been evaluated. We experimentally parasitized song sparrow (Melospiza melodia) nests with a brown-headed cowbird (Molothrus ater) chick to evaluate how host nestlings respond. Vocalizations emitted from experimentally parasitized nests were higher in frequency, and louder, than those from unparasitized nests, consistent with the cowbird exaggerating its signalling. In response, host nestlings exaggerated the frequency and amplitude of their vocalizations, such that they resembled the cowbird's while they 'scaled back' on calls per parental provisioning bout. Sparrows in parasitized nests were fed equally often as sparrows in unparasitized nests, suggesting that exaggerating some aspects of vocalization while scaling back on others can help host nestlings confronted with a cowbird. Our results support the recently proposed hypothesis that signalling in parasitized nests involves a dynamic interaction between parasitic and host nestlings, rather than a one-way process of mimicry by the parasite.     

Epigenetic effects of parasites and pesticides on captive and wild nestling birds

Anthropogenic changes to the environment challenge animal populations to adapt to new conditions and unique threats. While the study of adaptation has focused on genetic variation, epigenetic mechanisms may also be important. DNA methylation is sensitive to environmental stressors, such as parasites and pesticides, which may affect gene expression and phenotype. We studied the effects of an invasive ectoparasite, Philornis downsi, on DNA methylation of Galápagos mockingbirds (Mimus parvulus). We used the insecticide permethrin to manipulate P. downsi presence in nests of free‐living mockingbirds and tested for effects of parasitism on nestling mockingbirds using epiGBS, a reduced‐representation bisulfite sequencing (RRBS) approach. To distinguish the confounding effects of insecticide exposure, we conducted a matching experiment exposing captive nestling zebra finches (Taeniopygia guttata) to permethrin. We used zebra finches because they were the closest model organism to mockingbirds that we could breed in controlled conditions. We identified a limited number of differentially methylated cytosines (DMCs) in parasitized versus nonparasitized mockingbirds, but the number was not more than expected by chance. In contrast, we saw clear effects of permethrin on methylation in captive zebra finches. DMCs in zebra finches paralleled documented effects of permethrin exposure on vertebrate cellular signaling and endocrine function. Our results from captive birds indicate a role for epigenetic processes in mediating sublethal nontarget effects of pyrethroid exposure in vertebrates. Environmental conditions in the field were more variable than the laboratory, which may have made effects of both parasitism and permethrin harder to detect in mockingbirds. RRBS approaches such as epiGBS may be a cost‐effective way to characterize genome‐wide methylation profiles. However, our results indicate that ecological epigenetic studies in natural populations should consider the number of cytosines interrogated and the depth of sequencing in order to have adequate power to detect small and variable effects.     

Molecular tracking of individual host use in the Shiny Cowbird – a generalist brood parasite

Generalist parasites exploit multiple host species at the population level, but the individual parasite's strategy may be either itself a generalist or a specialist pattern of host species use. Here, we studied the relationship between host availability and host use in the individual parasitism patterns of the Shiny Cowbird Molothrus bonariensis, a generalist avian obligate brood parasite that parasitizes an extreme range of hosts. Using five microsatellite markers and an 1120‐bp fragment of the mtDNA control region, we reconstructed full‐sibling groups from 359 cowbird eggs and chicks found in nests of the two most frequent hosts in our study area, the Chalk‐browed Mockingbird Mimus saturninus and the House Wren Troglodytes aedon. We were able to infer the laying behavior of 17 different females a posteriori and found that they were mostly faithful to a particular laying area and host species along the entire reproductive season and did not avoid using previously parasitized nests (multiple parasitism) even when other nests were available for parasitism. Moreover, we found females using the same host nest more than once (repeated parasitism), which had not been previously reported for this species. We also found few females parasitizing more than one host species. The use of an alternative host was not related to the main hosts' nest availability. Overall, female shiny cowbirds use a spatially structured and host species specific approach for parasitism, but they do so nonexclusively, resulting in both detectable levels of multiple parasitism and generalism at the level of individual parasites.