Mekala Sundaram

Segregating the effects of seed traits and common ancestry of hardwood trees on eastern gray squirrel foraging decisions

The evolution of specific seed traits in scatter-hoarded tree species often has been attributed to granivore foraging behavior. However, the degree to which foraging investments and seed traits correlate with phylogenetic relationships among trees remains unexplored. We presented seeds of 23 different hardwood tree species (families Betulaceae, Fagaceae, Juglandaceae) to eastern gray squirrels (Sciurus carolinensis), and measured the time and distance travelled by squirrels that consumed or cached each seed. We estimated 11 physical and chemical seed traits for each species, and the phylogenetic relationships between the 23 hardwood trees. Variance partitioning revealed that considerable variation in foraging investment was attributable to seed traits alone (27–73%), and combined effects of seed traits and phylogeny of hardwood trees (5–55%). A phylogenetic PCA (pPCA) on seed traits and tree phylogeny resulted in 2 “global” axes of traits that were phylogenetically autocorrelated at the family and genus level and a third “local” axis in which traits were not phylogenetically autocorrelated. Collectively, these axes explained 30–76% of the variation in squirrel foraging investments. The first global pPCA axis, which produced large scores for seed species with thin shells, low lipid and high carbohydrate content, was negatively related to time to consume and cache seeds and travel distance to cache. The second global pPCA axis, which produced large scores for seeds with high protein, low tannin and low dormancy levels, was an important predictor of consumption time only. The local pPCA axis primarily reflected kernel mass. Although it explained only 12% of the variation in trait space and was not autocorrelated among phylogenetic clades, the local axis was related to all four squirrel foraging investments. Squirrel foraging behaviors are influenced by a combination of phylogenetically conserved and more evolutionarily labile seed traits that is consistent with a weak or more diffuse coevolutionary relationship between rodents and hardwood trees rather than a direct coevolutionary relationship.

The importance of including imperfect detection models in eDNA experimental design

Environmental DNA (eDNA) is DNA that has been isolated from field samples, and it is increasingly used to infer the presence or absence of particular species in an ecosystem. However, the combination of sampling procedures and subsequent molecular amplification of eDNA can lead to spurious results. As such, it is imperative that eDNA studies include a statistical framework for interpreting eDNA presence/absence data. We reviewed published literature for studies that utilized eDNA where the species density was known and compared the probability of detecting the focal species to the sampling and analysis protocols. Although biomass of the target species and the volume per sample did not impact detectability, the number of field replicates and number of samples from each replicate were positively related to detection. Additionally, increased number of PCR replicates and increased primer specificity significantly increased detectability. Accordingly, we advocate for increased use of occupancy modelling as a method to incorporate effects of sampling effort and PCR sensitivity in eDNA study design. Based on simulation results and the hierarchical nature of occupancy models, we suggest that field replicates, as opposed to molecular replicates, result in better detection probabilities of target species.

Population Decline in a Long-Lived Species: The Wood Turtle in Michigan

Abstract: Populations of Wood Turtles, Glyptemys insculpta, have steadily decreased over the past 30 yr because of habitat destruction and degradation. We sampled Wood Turtles from three areas in Michigan, USA, to characterize populations, quantify demographic trends, and measure the effect of declining population size on genetic diversity. Wood Turtle samples (n = 68) were collected from three rivers in the Lower Peninsula of Michigan and analyzed at nine microsatellite loci. Bayesian clustering programs identified two populations that split the three sampling sites into North and South populations. In both populations, analysis of genealogies estimated r < 0, indicating population decline. However, no evidence of a bottleneck was detected (P = 0.30 North, P = 0.29 South), and little evidence of inbreeding was observed (average North FIS = 0.25, average South FIS = 0.23), relative to other Emydidae populations. The high genetic diversity observed in the North and South populations is likely due to immigration between the two populations (FST = 0.04), coupled with the long life span of the Wood Turtle. The conflicting signals suggested from the genealogy models compared to the FIS and bottleneck analysis suggests that coalescent models may be better suited to detect population decline than other measures of genetic diversity in long-lived species such as the Wood Turtle.

Frequency-dependent hoarding by Sciurus carolinensis occurs with seeds of similar perceived value

Seed predation and rodent foraging behaviors depend on frequency of available seeds and seed traits. However, the interaction of frequency of seed availability and seed traits adds a new level of complexity to granivore–seed dynamics. We conducted experiments with eastern gray squirrels (Sciurus carolinensis) designed to elucidate the frequency × trait interaction. We hypothesized that frequency-dependent caching should occur only among pairs of seeds that are relatively similar in attributes that affect their perceived value as a storable food item. We also tested whether caching decisions were dependent on seeds already cached, a variable rarely considered in seed dispersal studies. Frequency-dependent seed caching occurred when seeds of relatively similar value (Juglans regia and Castanea mollissima) were paired. For this seed pair, caching decisions by S. carolinensis were dependent on seeds already cached such that squirrels tended to cache seeds that were either rare in the environment or in the cache. When seeds of very different caching values were paired (Juglans nigra and Corylus americana), a strong preference for the high-value seed was observed, but no frequency-dependent selection. We conclude that in pairings of seeds of differential caching value, the highly preferred seed is cached regardless of frequency of availability. In contrast, when seeds of similar value are paired, rarer (more common) seeds are cached at a higher (lower) rate than expected, and this behavior potentially stabilizes seed survival across available seed types leading to increased tree diversity. Our results indicate that caching of seeds by squirrels, and by implication recruitment of seedlings into plant populations, is likely driven by complex interactions between the relative frequency of seeds and their traits. We expect similar patterns to occur in any system in which foragers select among resource types that vary in perceived value.

Indirect evidence of prey-switching in minks: empirical evidence, theoretical modeling, and spatial drivers

Abstract A spatial gradient in the interactions between American minks (Neovison vison) and muskrats (Ondatra zibethicus) occurs in the Hudsons Bay Company fur harvest returns of Canada. Evidence for strong dependence of minks on muskrats exists in northwestern Canada, whereas evidence for weaker interactions exists in central and eastern Canada. We tested the hypothesis that minks consume fewer muskrats and more alternative prey in some areas, using fur records from 56 Hudsons Bay posts. Both muskrats and small microtines were found to explain mink dynamics, with small microtines and other alternative prey gaining importance in the eastern portion of our study area. Mink fur returns exhibited a range of cycle lengths from 2.6 to 13 years encompassing typical small microtine periodicities of 3–5 years and typical muskrat periodicities of 8–13 years. A time lag of 0 years occurred between mink and muskrat harvest data frequently in the eastern portion of our study area, hypothesized to be a result of minks consuming alternative prey. To biologically verify small microtines as a potential prey source, we modeled mink and muskrat population dynamics assuming small microtines were an alternative prey by modifying the Turchin and Hanski (1997) model. Simulated mink and muskrat time series replicated observed periodicity and time-lag range, suggesting that minks can be generalist predators and consume alternative prey. Finally, we examined species richness and land cover as potential drivers of mink prey-switching, but were unable to find support for either hypothesis, suggesting that additional environmental- or competition-related interactions influence mink population dynamics.

Eastern gray squirrels are consistent shoppers of seed traits: insights from discrete choice experiments

Seeds of many hardwood trees are dispersed by scatter-hoarding rodents, and this process is often mediated by the traits of seeds. Although numerous studies have linked seed traits to seed preference by rodents, little is known about how rodents forage for seeds when multiple desirable and undesirable seed traits are available simultaneously. Here, we adopt a novel method of designing choice experiments to study how eastern gray squirrels (Sciurus carolinensis) select for 6 traits (caloric value, protein content, tannin concentration, kernel mass, dormancy period and toughness of shell) among seeds. From n = 426 seed-pair presentations, we found that squirrels preferentially consumed seeds with short dormancy or tougher shells, and preferentially cached seeds with larger kernel mass, tougher shells and higher tannin concentrations. By incorporating random effects, we found that squirrels exhibited consistent preferences for seed traits, which is likely due to the fitness consequences associated with maintaining cached resources. Furthermore, we found that squirrels were willing to trade between multiple traits when caching seeds, which likely results in more seed species being cached in the fall. Ultimately, our approach allowed us to compute the relative values of different seed traits to squirrels, despite covariance among studied traits across seed species. In addition, by investigating how squirrels trade among different seed traits, important insights can be gleaned into behavioral mechanisms underlying seed caching (and, thus, seed survival) dynamics as well as evolutionary strategies adopted by plants to attract seed dispersers. We describe how discrete choice experiments can be used to study resource selection in other ecological systems.

Performance Benchmarks for Scholarly Metrics Associated with Fisheries and Wildlife Faculty.

Research productivity and impact are often considered in professional evaluations of academics, and performance metrics based on publications and citations increasingly are used in such evaluations. To promote evidence-based and informed use of these metrics, we collected publication and citation data for 437 tenure-track faculty members at 33 research-extensive universities in the United States belonging to the National Association of University Fisheries and Wildlife Programs. For each faculty member, we computed 8 commonly used performance metrics based on numbers of publications and citations, and recorded covariates including academic age (time since Ph.D.), sex, percentage of appointment devoted to research, and the sub-disciplinary research focus. Standardized deviance residuals from regression models were used to compare faculty after accounting for variation in performance due to these covariates. We also aggregated residuals to enable comparison across universities. Finally, we tested for temporal trends in citation practices to assess whether the “law of constant ratios”, used to enable comparison of performance metrics between disciplines that differ in citation and publication practices, applied to fisheries and wildlife sub-disciplines when mapped to Web of Science Journal Citation Report categories. Our regression models reduced deviance by ¼ to ½. Standardized residuals for each faculty member, when combined across metrics as a simple average or weighted via factor analysis, produced similar results in terms of performance based on percentile rankings. Significant variation was observed in scholarly performance across universities, after accounting for the influence of covariates. In contrast to findings for other disciplines, normalized citation ratios for fisheries and wildlife sub-disciplines increased across years. Increases were comparable for all sub-disciplines except ecology. We discuss the advantages and limitations of our methods, illustrate their use when applied to new data, and suggest future improvements. Our benchmarking approach may provide a useful tool to augment detailed, qualitative assessment of performance.