The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

Eggshell texture but not odor treatment affects model egg rejection in American robins (Turdus migratorius).

To curb fitness costs associated with obligate avian brood parasitism, some hosts have evolved to reject foreign eggs in the nest. American robins (Turdus migratorius) are among the few hosts of the brown-headed cowbird (Molothrus ater) that mostly remove parasitic eggs from their nests. With the parasite's eggs looking nothing like their own, American robins likely rely most on visual cues when making rejection decisions. However, we still know little about the roles that tactile and olfactory cues play in robin's or other rejecter hosts' rejection decisions. Here, we conducted a set of experiments to test for the use of tactile or olfactory cues in egg rejection by robins. For the tactile experiment, we found that robins were more likely to reject rough rather than smooth eggs. However, our tactile model egg design was not able to fully discriminate between tactile and visual sensory modalities. In the olfaction experiment, we did not find a significant effect of egg scent treatment on rejection rates. Accordingly, future studies on egg rejection should attempt to fully distinguish between tactile and visual cues, as well as examine olfactory cues in other egg rejecter host species.

The effect of avian brood parasitism on physiological responses of host nestlings.

Avian obligate brood parasites lay their eggs in the nests of other species that may provide care for the foreign offspring. Brood parasitism often imparts substantial fitness losses upon host nestlings when they are raised alongside the typically more competitive, larger, and older parasitic chick(s). Whereas fitness costs due to reduced host offspring survival in parasitized broods have been studied in detail, the physiological changes in host nestlings caused by parasitic nestmate(s) are less well known. We compared prothonotary warbler (Protonotaria citrea) nestlings, a host of the nest-sharing brown-headed cowbird (Molothrus ater), in experimentally parasitized vs. non-parasitized broods. Our aim was to determine whether cohabitation with brood parasitic young impacted host nestling baseline corticosterone plasma concentrations, immune responses, body condition, and mortality. Corticosterone levels and body condition of host nestlings were similar between nests with or without a cowbird nestmate, whereas host immune responses were lower and nestling mortality was greater in parasitized broods, irrespective of variation in brood size or total brood mass. We detected no trade-offs of baseline corticosterone levels with either immune responses or with body condition. These results suggest that this host species' nestlings experience some adverse fitness-relevant physiological effects in parasitized broods, but are also resilient in other aspects when coping with brood parasitism.

Physiological responses of host parents to rearing an avian brood parasite: An experimental study.

Raising an obligate avian brood parasite is costly for host parents because it redirects valuable parental resources from one's own offspring to genetically unrelated young. The costs of raising a brood parasite may be mediated by physiological stressors for foster parents if it requires greater or biased parental effort compared to raising non-parasitized broods. For example, upregulating glucocorticoid hormones or reducing immune responses may mediate a trade-off between resource allocation to a current brood versus future reproductive opportunities, but published data on parasitized hosts' physiology are scarce. Here we used an experimental approach to test if host parents respond to the presence of brood parasitic young through dynamic changes in their own physiology. We conducted our experiments with parasitic brown-headed cowbirds (Molothrus ater) fostered into nests of host prothonotary warblers (Protonotaria citrea). Relative to parents caring for non-parasitized control broods, parasitism increased baseline corticosterone levels and reduced body mass in adult male, but not in female, hosts. Immune responses to a novel antigen were depressed in both parents of parasitized broods compared to parents of non-parasitized broods. Additionally, we found that immune function increased along the breeding season regardless of treatment. These experiments also confirmed prior observational data that parasitized adult males have reduced return rates to breeding sites in years subsequent to raising cowbirds. The findings demonstrate diverse physiological effects of parasitism on the foster parents in our particular host-brood parasite system, yet we found no evidence of individual trade-offs between endocrine and immune responses of adult hosts.

Greater opportunities for sexual selection in male than in female obligate brood parasitic birds.

Females are expected to have evolved to be more discriminatory in mate choice than males as a result of greater reproductive investment into larger gametes (eggs vs. sperm). In turn, males are predicted to be more promiscuous than females, showing both a larger variance in the number of mates and a greater increase in reproductive success with more mates, yielding more intense sexual selection on males vs. females (Bateman's Paradigm). However, sex differences in costly parental care strategies can either reinforce or counteract the initial asymmetry in reproductive investment, which may be one cause for some studies failing to conform with predictions of Bateman's Paradigm. For example, in many bird species with small female-biased initial investment but extensive biparental care, both sexes should be subject to similar strengths of sexual selection because males and females are similarly restricted in their ability to pursue additional mates. Unlike 99% of avian species, however, obligate brood parasitic birds lack any parental care in either sex, predicting a conformation to Bateman's Paradigm. Here we use microsatellite genotyping to demonstrate that in brood parasitic brown-headed cowbirds (Molothrus ater), per capita annual reproductive success increases with the number of mates in males, but not in females. Furthermore, also as predicted, the variance of the number of mates and offspring is greater in males than in females. Thus, contrary to previous findings in this species, our results conform to predictions of the Bateman's Paradigm for taxa without parental care.

A generalist brood parasite modifies use of a host in response to reproductive success.

Avian obligate brood parasites, which rely solely on hosts to raise their young, should choose the highest quality hosts to maximize reproductive output. Brown-headed cowbirds (Molothrus ater) are extreme host generalists, yet female cowbirds could use information based on past reproductive outcomes to make egg-laying decisions thus minimizing fitness costs associated with parasitizing low-quality hosts. We use a long-term (21 years) nest-box study of a single host, the prothonotary warbler (Protonotaria citrea), to show that local cowbird reproductive success, but not host reproductive success, was positively correlated with the probability of parasitism the following year. Experimental manipulations of cowbird success corroborated that female cowbirds make future decisions about which hosts to use based on information pertaining to past cowbird success, both within and between years. The within-year pattern, in particular, points to local cowbird females selecting hosts based on past reproductive outcomes. This, coupled with high site fidelity of female cowbirds between years, points to information use, rather than cowbird natal returns alone, increasing parasitism rates on highly productive sites between years.

Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds.

Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host's egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts.

The limits of egg recognition: testing acceptance thresholds of American robins in response to decreasingly egg-shaped objects in the nest.

Some hosts of avian brood parasites reduce or eliminate the costs of parasitism by removing foreign eggs from the nest (rejecter hosts). In turn, even acceptor hosts typically remove most non-egg-shaped objects from the nest, including broken shells, fallen leaves and other detritus. In search for the evolutionary origins and sensory mechanisms of egg rejection, we assessed where the potential threshold between egg recognition and nest hygiene may lie when it comes to stimulus shape. Most previous studies applied comparisons of egg-sized objects with non-continuous variation in shape. Here, instead, we used two series of three-dimensional-printed objects, designed a priori to increasingly diverge from natural eggs along two axes (width or angularity) of shape variation. As predicted, we detected transitions from mostly acceptance to mostly rejection in the nests of American robins Turdus migratorius along each of the two axes. Our methods parallel previous innovations in egg-rejection studies through the use of continuous variation in egg coloration and maculation contrast, to better understand the sensory limits and thresholds of variation in egg recognition and rejection in diverse hosts of avian brood parasites.

Brood Parasites Are a Heterogeneous and Functionally Distinct Class of Natural Enemies.

Brood parasitism is the introduction of unrelated progeny into the nest or colony of a host that then raises the foreign young. This reproductive strategy has evolved independently and repeatedly among diverse animal taxa, and brood parasite-host interactions have become models for understanding coevolutionary arms races. Yet brood parasites have remained largely overlooked in previous syntheses of natural enemy ecology. Here, we argue that brood parasites are a heterogeneous and versatile class of natural enemies, blending traits characteristic of predators and trophic parasites. The functional distinctness of brood parasites reinforces the idea that natural enemies exist along a continuum rather than as a dichotomy. Brood parasite-host interactions can serve as valuable case studies to unify parasite-host and predator-prey theories.

Using Digital Image Analysis to Quantify Small Arthropod Vectors.

Quantifying arthropod vectors can be a time-consuming process. Here, we describe a technique to count large samples of small arthropods using ImageJ. ImageJ is an open source image processing software, produced by the National Institutes of Health, with a straightforward interface that has proven useful in quantifying small organisms (i.e., cells, pollen, eggs). In 2017, we deployed CDC light traps baited with carbon dioxide among seven sites to capture black flies (Diptera: Simuliidae). Samples of the captured specimens were photographed, and then quantified manually and automatically, using ImageJ. We compared the accuracy of three types of automated counts to manual counts of black flies using an information-theoretic approach. We found that changing the particle size produced counts closest to those obtained by manual counts. Even over a large range of values, from tens to thousands of flies, our automated counts were often identical to and almost always within 5% of the manual counts. When different, automated counts were usually slightly less than manual counts, and thus conservative estimates. This automated technique is simple, repeatable, requires minimal training, and can reduce the time needed to quantify small arthropods such as black flies.

Juvenile survival in a neotropical migratory songbird is lower than expected.

Attempts to estimate and identify factors influencing first-year survival in passerines, survival between fledging and the first reproductive attempt (i.e. juvenile survival), have largely been confounded by natal dispersal, particularly in long-distance migratory passerines. We studied Prothonotary Warblers (Protonotaria citrea) breeding in nest boxes to estimate first-year survival while accounting for biases related to dispersal that are common in mark-recapture studies. The natal dispersal distribution (median = 1420 m; n = 429) and a distance-dependent recruitment rate, which controls for effects of study site configuration, both indicated a pattern of short-distance natal dispersal. This pattern was consistent with results of a systematic survey for birds returning outside the nest box study sites (up to 30 km in all directions) within a majority (81%) of total available bottomland forest habitat, further suggesting that permanent emigration outside of the study system was rare. We used multistate mark-recapture modeling to estimate first-year survival and incorporated factors thought to influence survival while accounting for the potential confounding effects of dispersal on recapture probabilities for warblers that fledged during 2004-2009 (n = 6093). Overall, the average first-year survival for warblers reared without cowbird nestmates was 0.11 (95% CI = 0.09-0.13), decreased with fledging date (0.22 early to 0.03 late) and averaged 40% lower for warblers reared with a brood parasite nestmate. First-year survival was less than half of the rate thought to represent population replacement in migratory passerines (∼0.30). This very low rate suggests that surviving the first year of life for many Neotropical migratory species is even more difficult than previously thought, forcing us to rethink estimates used in population models.

Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs.

Why do many hosts accept costly avian brood parasitism even when parasitic eggs and nestlings differ dramatically in appearance from their own? Scientists argue that evolutionary lag or equilibrium can explain this evolutionary enigma. Few, however, consider the potential of parasitic birds to enforce acceptance by destroying eggs or nestlings of hosts that eject parasitic eggs and thereby reject parasitism. This retaliatory "mafia" behavior has been reported in one species of parasitic cuckoo but never in parasitic cowbirds. Here we present experimental evidence of mafia behavior in the brown-headed cowbird (Molothrus ater), a widely distributed North American brood parasite. We manipulated ejection of cowbird eggs and cowbird access to predator-proof nests in a common host to test experimentally for mafia behavior. When cowbird access was allowed, 56% of "ejector" nests were depredated compared with only 6% of "accepter" nests. No nests were destroyed when cowbird access was always denied or when access was denied after we removed cowbird eggs, indicating that cowbirds were responsible. Nonparasitized nests were depredated at an intermediate rate (20%) when cowbirds were allowed access, suggesting that cowbirds may occasionally "farm" hosts to create additional opportunities for parasitism. Cowbirds parasitized most (85%) renests of the hosts whose nests were depredated. Ejector nests produced 60% fewer host offspring than accepter nests because of the predatory behavior attributed to cowbirds. Widespread predatory behaviors in cowbirds could slow the evolution of rejection behaviors and further threaten populations of some of the >100 species of regular cowbird hosts.

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.

Brood parasitism increases provisioning rate, and reduces offspring recruitment and adult return rates, in a cowbird host.

Interspecific brood parasitism in birds presents a special problem for the host because the parasitic offspring exploit their foster parents, causing them to invest more energy in their current reproductive effort. Nestling brown-headed cowbirds (Molothrus ater) are a burden to relatively small hosts and may reduce fledgling quality and adult survival. We documented food-provisioning rates of one small host, the prothonotary warbler (Protonotaria citrea), at broods that were similar in age (containing nestlings 8-9 days old), but that varied in composition (number of warbler and cowbird nestlings) and mass, and measured the effect of brood parasitism on offspring recruitment and adult returns in the host. The rate of food provisioning increased with brood mass, and males and females contributed equally to feeding nestlings. Controlling for brood mass, the provisioning rate was higher for nests with cowbirds than those without. Recruitment of warbler fledglings from unparasitized nests was 1.6 and 3.7 times higher than that of fledglings from nests containing one or two cowbirds, respectively. Returns of double-brooded adult male and female warblers decreased with an increase in the number of cowbirds raised, but the decrease was more pronounced in males. Reduced returns of warbler adults and recruitment of warbler fledglings with increased cowbird parasitism was likely a result of reduced survival. Cowbird parasitism increased the warblers' investment in current reproductive effort, while exerting additional costs to current reproduction and residual reproductive value. Our study provides the strongest evidence to date for negative effects of cowbird parasitism on recruitment of host fledglings and survival of host adults.