Climatic and geographic predictors of life history variation in Eastern Massasauga (Sistrurus catenatus): A range-wide synthesis.

Elucidating how life history traits vary geographically is important to understanding variation in population dynamics. Because many aspects of ectotherm life history are climate-dependent, geographic variation in climate is expected to have a large impact on population dynamics through effects on annual survival, body size, growth rate, age at first reproduction, size-fecundity relationship, and reproductive frequency. The Eastern Massasauga (Sistrurus catenatus) is a small, imperiled North American rattlesnake with a distribution centered on the Great Lakes region, where lake effects strongly influence local conditions. To address Eastern Massasauga life history data gaps, we compiled data from 47 study sites representing 38 counties across the range. We used multimodel inference and general linear models with geographic coordinates and annual climate normals as explanatory variables to clarify patterns of variation in life history traits. We found strong evidence for geographic variation in six of nine life history variables. Adult female snout-vent length and neonate mass increased with increasing mean annual precipitation. Litter size decreased with increasing mean temperature, and the size-fecundity relationship and growth prior to first hibernation both increased with increasing latitude. The proportion of gravid females also increased with increasing latitude, but this relationship may be the result of geographically varying detection bias. Our results provide insights into ectotherm life history variation and fill critical data gaps, which will inform Eastern Massasauga conservation efforts by improving biological realism for models of population viability and climate change.

Do seasonal patterns of rat snake (Pantherophis obsoletus) and black racer (Coluber constrictor) activity predict avian nest predation?

Avian nest success often varies seasonally and because predation is the primary cause of nest failure, seasonal variation in predator activity has been hypothesized to explain seasonal variation in nest success. Despite the fact that nest predator communities are often diverse, recent evidence from studies of snakes that are nest predators has lent some support to the link between snake activity and nest predation. However, the strength of the relationship has varied among studies. Explaining this variation is difficult, because none of these studies directly identified nest predators, the link between predator activity and nest survival was inferred. To address this knowledge gap, we examined seasonal variation in daily survival rates of 463 bird nests (of 17 bird species) and used cameras to document predator identity at 137 nests. We simultaneously quantified seasonal activity patterns of two local snake species (N = 30 individuals) using manual (2136 snake locations) and automated (89,165 movements detected) radiotelemetry. Rat snakes (Pantherophis obsoletus), the dominant snake predator at the site (~28% of observed nest predations), were most active in late May and early June, a pattern reported elsewhere for this species. When analyzing all monitored nests, we found no link between nest predation and seasonal activity of rat snakes. When analyzing only nests with known predator identities (filmed nests), however, we found that rat snakes were more likely to prey on nests during periods when they were moving the greatest distances. Similarly, analyses of all monitored nests indicated that nest survival was not linked to racer activity patterns, but racer-specific predation (N = 17 nests) of filmed nests was higher when racers were moving the greatest distances. Our results suggest that the activity of predators may be associated with higher predation rates by those predators, but that those effects can be difficult to detect when nest predator communities are diverse and predator identities are not known. Additionally, our results suggest that hand-tracking of snakes provides a reliable indicator of predator activity that may be more indicative of foraging behavior than movement frequency provided by automated telemetry systems.

Power lines, roads, and avian nest survival: effects on predator identity and predation intensity.

1 Anthropogenic alteration of landscapes can affect avian nest success by influencing the abundance, distribution, and behavior of predators. Understanding avian nest predation risk necessitates understanding how landscapes affect predator distribution and behavior. 2 From a sample of 463 nests of 17 songbird species, we evaluated how landscape features (distance to forest edge, unpaved roads, and power lines) influenced daily nest survival. We also used video cameras to identify nest predators at 137 nest predation events and evaluated how landscape features influenced predator identity. Finally, we determined the abundance and distribution of several of the principal predators using surveys and radiotelemetry. 3 Distance to power lines was the best predictor of predator identity: predation by brown-headed cowbirds (Molothrus ater), corvids (Corvus sp. and Cyanocitta cristata), racers (Coluber constrictor), and coachwhips (Masticophis flagellum) increased with proximity to power lines, whereas predation by rat snakes (Elaphe obsoleta) and raptors decreased. In some cases, predator density may reliably indicate nest predation risk because racers, corvids, and cowbirds frequently used power line right-of-ways. 4 Of five bird species with enough nests to analyze individually, daily nest survival of only indigo buntings (Passerina cyanea) decreased with proximity to power lines, despite predation by most predators at our site being positively associated with power lines. For all nesting species combined, distance to unpaved road was the model that most influenced daily nest survival. This pattern is likely a consequence of rat snakes, the locally dominant nest predator (28% of predation events), rarely using power lines and associated areas. Instead, rat snakes were frequently associated with road edges, indicating that not all edges are functionally similar. 5 Our results suggest that interactions between predators and landscape features are likely to be specific to both the local predators and landscape. Thus, predicting how anthropogenic changes to landscapes affect nesting birds requires that we know more about how landscape changes affect the behavior of nest predators and which nest predators are locally important.

Implications of spatial patterns of roosting and movements of American robins for West Nile virus transmission.

The arrival of West Nile virus (WNV) in North America has led to interest in the interaction between birds, the amplification hosts of WNV, and Culex mosquitoes, the primary WNV vectors. American robins (Turdus migratorius) are particularly important amplification hosts of WNV, and because the vector Culex mosquitoes are primarily nocturnal and feed on roosting birds, robin communal roosting behavior may play an important role in the transmission ecology of WNV. Using data from 43 radio-tracked individuals, we determined spatial and temporal patterns of robin roosting behavior, and how these patterns related to the distribution of WNV-infected mosquitoes. Use of the communal roost and fidelity to foraging areas was highly variable both within and among individual robins, and differed markedly from patterns documented in a previous study of robin roosting. Although there were clear seasonal patterns to both robin roosting and WNV occurrence, there was no significant relationship between communal roosting by robins and temporal or spatial patterns of WNV-positive mosquitoes. Our results suggest that, although robins may be important as WNV hosts, communal roosts are not necessarily important for WNV amplification. Other factors, including the availability and distribution of high-quality mosquito habitat and favorable weather for mosquito reproduction, may influence the importance of robin roosts for local WNV amplification and transmission.

Latitudinal variation in seasonal activity and mortality in ratsnakes (Elaphe obsoleta).

The ecology of ectotherms should be particularly affected by latitude because so much of their biology is temperature dependent. Current latitudinal patterns should also be informative about how ectotherms will have to modify their behavior in response to climate change. We used data from a total of 175 adult black ratsnakes (Elaphe obsoleta) radio-tracked in Ontario, Illinois, and Texas, a latitudinal distance of >1500 km, to test predictions about how seasonal patterns of activity and mortality should vary with latitude. Despite pronounced differences in temperatures among study locations, and despite ratsnakes in Texas not hibernating and switching from diurnal to nocturnal activity in the summer, seasonal patterns of snake activity were remarkably similar during the months that snakes in all populations were active. Rather than being a function of temperature, activity may be driven by the timing of reproduction, which appears similar among populations. Contrary to the prediction that mortality should be highest in the most active population, overall mortality did not follow a clinal pattern. Winter mortality did increase with latitude, however, consistent with temperature limiting the northern distribution of ratsnakes. This result was opposite that found in the only previous study of latitudinal variation in winter mortality in reptiles, which may be a consequence of whether or not the animals exhibit true hibernation. Collectively, these results suggest that, at least in the northern part of their range, ratsnakes should be able to adjust easily to, and may benefit from, a warmer climate, although climate-based changes to the snakes' prey or habitat, for example, could alter that prediction.

Linking snake behavior to nest predation in a Midwestern bird community.

Nest predators can adversely affect the viability of songbird populations, and their impact is exacerbated in fragmented habitats. Despite substantial research on this predator-prey interaction, however, almost all of the focus has been on the birds rather than their nest predators, thereby limiting our understanding of the factors that bring predators and nests into contact. We used radiotelemetry to document the activity of two snake species (rat snakes, Elaphe obsoleta; racers, Coluber constrictor) known to prey on nests in Midwestern bird communities and simultaneously monitored 300 songbird nests and tested the hypothesis that predation risk should increase for nests when snakes were more active and in edge habitat preferred by both snake species. Predation risk increased when rat snakes were more active, for all nests combined and for two of the six bird species for which we had sufficient nests to allow separate analyses. This result is consistent with rat snakes being more important nest predators than racers. We found no evidence, however, that nests closer to forest edges were at greater risk. These results are generally consistent with the one previous study that investigated rat snakes and nest predation simultaneously. The seemingly paradoxical failure to find higher predation risk in the snakes' preferred habitat (i.e., edge) might be explained by the snakes using edges at least in part for non-foraging activities. We propose that higher nest predation in fragmented habitats (at least that attributable to snakes) results indirectly from edges promoting larger snake populations, rather than from edges directly increasing the risk of nest predation by snakes. If so, the notion of edges per se functioning as ecological "traps" merits further study.

Seasonal sex allocation by Common Grackles? Revisiting a foundational study.

Despite the general importance of replication in science, relatively few behavioral ecology studies are repeated. Here we repeat the seminal 1977 research of H. F. Howe, who found that the proportion of male nestlings at hatching in nests of Common Grackles (Quiscalus quiscula) increased as the breeding season progressed. Howe interpreted this pattern as an adaptive response to changing food conditions that favored greater production of daughters (the sex less expensive to rear) when food was scarce and sons when food was more abundant. Using DNA-based sexing and larger samples, we found no evidence of nonrandom seasonal sex allocation and no evidence that sons were more vulnerable to starvation than daughters. These patterns also prevailed among renesting efforts late in the season, when starvation was extreme. Although there is no way to exclude the possibility that grackles employed different sex allocation tactics in the two studies, similarities in weather, habitat, nesting phenology, and starvation rates make it seem unlikely that ecological differences between our study and Howe's explain the disparate results, whereas failure of assumptions that Howe was unable to test seems more plausible.

Prey-mediated effects of drought on condition and survival of a terrestrial snake.

Drought can have severe ecological effects and global climate-change theory predicts that droughts are likely to increase in frequency and severity. Therefore, it is important that we broaden our understanding of how drought affects not only individual species, but also multitrophic interactions. Here we document vegetation and small-mammal abundance and associated patterns of Texas ratsnake (Elaphe obsoleta) body condition and survival before, during, and after a drought in central Texas, USA. Vegetation (grass and forbs) height and small-mammal capture rates were two times greater in wet years compared to the drought year. The decline of small mammals (the snakes' principal prey) during the drought was associated with a drop in ratsnake body condition, consistent with reduced food intake. During the drought, snake mortality also increased 24%. Although higher snake mortality was attributable to predation and road mortality rather than being a direct result of starvation, an increase in risk-prone behavior by foraging snakes probably increased their exposure to those other mortality factors. Drought conditions lasted only for 21 months, and vegetation, small-mammal abundance, and snake condition had returned to pre-drought levels within a year. Although estimates of snake population size were not available, it is likely that substantially more than a year was required for the population to return to its previous size.

Energetics and space use: intraspecific and interspecific comparisons of movements and home ranges of two Colubrid snakes.

1. Energy requirements explain substantial variation in movement and home range size among birds and mammals. This study assesses whether the same is true of snakes by comparing ratsnakes (Elaphe obsoleta) and racers (Coluber constrictor), ecologically similar species whose energy requirements appear to differ substantially (racers > ratsnakes). 2. Over 4 years 22 Elaphe and 16 Coluber were radio-tracked at the same site in Illinois to examine how movement and home ranges varied by sex and season. 3. Coluber moved more often and further per move than Elaphe, resulting in their estimated mean day range being almost four times larger than that of Elaphe (88.0 m day(-1) vs. 23.1 m day(-1)). 4. Both male and female Elaphe moved more frequently early in the season consistent with mate-searching, but mean distances moved did not differ seasonally or by sex. Both sexes of Coluber moved more later in the season and overall males moved further than females. 5. Interspecifically, patterns were consistent with the energetics hypothesis--Coluber had mean home ranges approximately four times larger than those of Elaphe. 6. Intraspecifically, increased movement did not always produce larger home ranges. Male Elaphe had larger home ranges than females despite not moving further, whereas male Coluber had comparable home ranges to females despite moving further. Also, Elaphe home ranges in Illinois were substantially smaller than has been documented in Ontario, despite Ontario Elaphe moving less. 7. Our results generally support the energetics hypothesis, but indicate that knowledge of ecology and energetics increases our understanding of area requirements beyond simple allometric predictions.

Egg size variation in birds with asynchronous hatching: is bigger really better?

In many animals large size at birth enhances offspring survival, but comparative evidence remains equivocal for birds. Failure to consider asynchronous hatching (ASH) may have confounded previous analyses. We assessed effects of egg size and ASH on growth and survival of common grackle (Quiscalus quiscula) nestlings to test the hypothesis that females adjust the size of last-laid eggs to modify effects of ASH. Although positive, the effect of egg size on nestling growth and survival was overwhelmed by the effect of ASH, with late-hatched nestlings being most likely to starve. Egg size did significantly affect growth late in the nestling period, but only because starvation had greatly reduced hatching asynchrony among surviving nestlings. Similarly, in experimentally synchronized nests, egg size and hatching asynchrony both affected offspring growth early in the nestling phase. Our results suggest that there is unlikely to be an adaptive advantage to females from varying the size of last-laid eggs in species with substantial ASH and that studies to assess the effect of a given maternal effect (e.g., varying egg size) should be done in the context of other maternal effects that may be operating simultaneously (e.g., ASH).

Hybridization between mtDNA-defined phylogeographic lineages of black ratsnakes (Pantherophis sp.).

Phylogeographic analyses using mitochondrial DNA (mtDNA) have revealed many examples of apparently deep historical subdivisions ('phylogroups') within many vertebrates. It remains unclear whether these phylogroups represent independently evolving, adaptively differentiated lineages or groups that show little functional differentiation and, hence, will merge on contact. Here, we use mtDNA sequence data to evaluate the phylogeographic relationships between two of the northernmost populations of black ratsnakes (Pantherophis obsoletus complex) in Ontario, Canada and previously analysed populations in the United States. We then use population-level analyses to evaluate the level of adaptive divergence between previously established mtDNA phylogroups. Phylogenetic analyses show that southern Ontario snakes have mtDNA haplotypes that fall within the Central mtDNA phylogroup, as designated by Burbrink et al. (2000). In contrast, snakes in eastern Ontario carry either Central or Eastern-specific haplotypes. Within the hybrid region, we found highly variable frequencies of mtDNA haplotypes among isolated sub-populations, no association between variation in cytonuclear (mtDNA) and nuclear (microsatellite DNA) markers, no difference in survival or reproductive success among snakes with different mtDNA haplotypes, and no effect of mate similarity in mtDNA on female clutch size. These results argue that the Eastern and Central phylogroups have merged in this region, likely due to a lack of adaptive differentiation between individuals in each lineage. Hence, in these snakes, phylogeographic structure in mtDNA is more a reflection of historical isolation rather than adaptive divergence. The observed reticulation between lineages and lack of evidence for hybrid disgenesis also bears on the classification of these lineages as distinct species.

Energetics of parental care in six syntopic centrarchid fishes.

We studied parental behavior in six syntopically breeding species of centrarchid fishes to determine whether energetic costs could contribute to our understanding of the diversity of parental care. We used a combination of underwater videography, radio telemetry and direct observation to examine how the cost of parental care varied with both its duration and intensity. Duration of parental care, activity patterns, and energetic costs varied widely among species. Overall, the duration of care increased with parental size between species. When energetic costs were adjusted for species-specific differences in the duration of parental care, the cost of parental care also increased with mean size of the species. Species with extended parental care exhibited stage-specific patterns of activity and energy expenditure consistent with parental investment theory, whereas fish with short duration parental care tended to maintain high levels of activity throughout the entire period of parental care. The only apparent exception (a species with brief parental care but stage-specific behavior) was a species with multiple breeding bouts, and thus effectively having protracted parental care. These data suggest that some species with short duration parental care can afford not to adjust parental investment over stages of offspring development. Using our empirical data on parental care duration and costs, we reevaluated the relationship between egg size and quality of parental care. Variation in egg size explained almost all of the observed variation in total energetic cost of parental care, and to a lesser degree, duration-the larger the eggs, the more costly the parental care. This research highlights the value of incorporating energetic information into the study of parental care behavior and testing of ecological theory.

Long-term decline in a red-winged blackbird population: ecological causes and sexual selection consequences.

Habitat loss and large-scale climate phenomena are widely implicated as causing decline in animal populations. I examined how both factors contributed to a precipitous decline in an Ontario red-winged blackbird (Agelaius phoeniceus) population using 16 years of data collected between 1974 and 1995. The decline was manifested as an almost 50% reduction in mean harem size, which reduced the opportunity for sexual selection threefold. Regional hay production, which should affect recruitment into the study population, also declined substantially. Correlation between blackbirds and hay may be coincidental, however, because annual changes in harem size were not associated with annual changes in hay production. This study coincided with an unprecedented positive phase of the North Atlantic Oscillation (NAO). Changes in harem size were correlated with winter NAO index values, suggesting that winter mortality contributed to the population decline. Positive correlation between harem size change and male return rates also supported the winter mortality hypothesis. Continued declines will cause this blackbird population to change from socially polygynous to socially monogamous. Study of red-winged blackbird winter ecology is needed to identify the proximate causes of mortality, whereas breeding studies can explore the consequences of relaxed sexual selection.

Effects of climate variation on timing of nesting, reproductive success, and offspring sex ratios of red-winged blackbirds.

Predicting ecological consequences of climate change will be improved by understanding how species are affected by contemporary climate variation, particularly if analyses involve more than single ecological variables and focus on large-scale climate phenomena. I used 18 years of data from red-winged blackbirds (Agelaius phoeniceus) studied over a 25-year period in eastern Ontario to explore chronological and climate-related patterns of reproduction. Although blackbirds started nesting earlier in years with warmer springs, associated with low winter values of the North Atlantic Oscillation Index (NAOI), there was no advance in laying dates over the study. Nesting ended progressively later and the breeding season lasted longer over the study, however, associated with higher spring values of NAOI. As the length of the nesting season increased, offspring sex ratios became more female biased, apparently as a result of females adjusting the sex of the eggs they laid, rather than from sex-biased nestling mortality. Clutch size did not vary systematically over the study or with climate. Opposing trends of declining nest success and increasing productivity of successful nests over the study resulted in no chronological change in productivity per female. Higher productivity of successful nests was associated with higher winter NAOI values, possibly because synchrony between nesting and food availability was higher in years with high NAOI values. Other than the association between the start of nesting and spring temperatures, local weather (e.g., temperature, rainfall) patterns that linked NAOI with reproduction were not identified, suggesting that weather patterns may be complex. Because climate affected most aspects of red-winged blackbird reproduction examined, focusing on associations between climate and single variables (e.g., first-egg dates) will have limited value in predicting how future climates will affect populations.

HIERARCHICAL PATTERNS OF GENETIC POPULATION STRUCTURE IN BLACK RAT SNAKES (ELAPHE OBSOLETA OBSOLETA) AS REVEALED BY MICROSATELLITE DNA ANALYSIS.

We investigated the distribution of variation at six microsatellite loci in the black rat snake (Elaphe obsoleta obsoleta). Sampling occurred at three hierarchical scales ranging from communal hibernacula to regional populations, with most locales situated within the Frontenac Axis region of eastern Ontario. We detected no statistically significant pairwise differentiation (FST and RST ) between hibernacula within the same subpopulations (interhibernaculum distance <6 km). However, isolation-by-distance was evident among locales within the Frontenac Axis (maximum of 50 km) and among regional populations (maximum of 1500 km). Conservative estimates of Nc derived from heterozygosity values ranged from approximately 600 to 2000. These values suggest relatively large genetic neighborhoods encompassing many communal hibernacula. Our results considered together suggest viscosity of gene flow over relatively short distances (tens of kilometers), but substantial genetic exchange among local hibernacula.

NATURAL SELECTION AND SEXUAL SIZE DIMORPHISM IN RED-WINGED BLACKBIRDS.

Patterns of overwinter mortality in the sexually dimorphic red-winged blackbird (Agelaius phoeniceus) were examined to test the predictions of the sexual-selection hypothesis that male size is limited by directional selection favoring small males and that female size is maintained by stabilizing selection wherein extreme phenotypes experience higher mortality. Museum specimens collected from Ontario over a 95-yr period were used to compare the sizes of males and females collected in fall and spring. In a separate field study, body sizes of returning and nonreturning male and female red-winged blackbirds were compared over a 6-yr period. Overall, there was no evidence of higher overwinter mortality among larger males. Among adult (ASY) males, large individuals appeared to have higher survival than small individuals, although among subadult (SY) males, large size may have been disadvantageous. Weak evidence of stabilizing selection on female body size was found. Among adults, sexual size dimorphism seemed more pronounced after winter than before winter. Our results do not support the hypothesis that body size in male red-winged blackbirds is limited by selective mortality outside the breeding season. It is possible that size selection occurs earlier in life, when males are still in the nest. Our results suggest that caution should be exercised when interpreting interspecific evidence showing higher adult male than female mortality in sexually dimorphic species. Such patterns could arise as a cost to males of sexual selection and yet provide no insight into how natural selection opposes sexual selection for increased male size.

SEXUAL SIZE DIMORPHISM AND EGG-SIZE ALLOMETRY IN BIRDS.

We tested the hypothesis that egg size should evolve in sexually dimorphic birds to reduce costs associated with more rapid growth by nestlings of the larger sex. Consistent with this hypothesis, we found that in species in which males were larger, females laid proportionately larger eggs as sexual size dimorphism increased. However, this result was also consistent with the hypothesis that egg size varied allometrically with both male and female body size. Furthermore we found that in species in which females were larger, relative egg size decreased as size dimorphism increased, which is consistent with the "allometry hypothesis" but not the "cost-reduction hypothesis. That male body size contributes to the allometric relationship between egg size and body size suggests that the basis for the allometric relationship is not wholly a mechanical one stemming from the physical requirements of developing, transporting, and laying an egg of a particular size. Rather, the relationship seems likely to be tied more directly to body size itself the tact that male body size influences a female trait suggests that egg size-body size relationships otter some scope for investigating the basis for allometric relationships in general.

TARGETS OF SEXUAL SELECTION: SONG AND PLUMAGE OF WOOD WARBLERS.

Extant hypotheses predict that, in the face of sexual selection, avian song and plumage may evolve in a concerted fashion, in an antagonistic fashion, or in ways unrelated to each other. To test these ideas regarding which traits sexual selection targets, and the consequences for other traits, we analyzed patterns of song complexity and plumage dimorphism in 56 species of wood warblers (Parulinae). Overall, males of more dimorphic species sang shorter songs more often, but did not have more complex songs. However, when monomorphic species were excluded from the analysis, we found that the total time spent singing and repertoire size increased with plumage dimorphism. Monomorphic species are predominantly ground-nesters and the greater risk of nest predation for these species may constrain males from becoming more visually conspicuous. Thus, sexual selection may have been restricted to targeting song in these species. Even though song may have been the only target of sexual selection in ground-nesting species, overall, song in those species is not more complex than in species that nest above the ground. We propose that traits targeted by sexual selection evolve in concert, except when constrained by some ecological factor.