Predator morphology affects prey consumption: evidence from an anuran population in subtropical wetlands

The expansion, densification and proliferation of urban areas around the world is currently occurring at a rate that is unprecedented in human history. It is predicted that global urban land cover will triple between 2000 and 2030, with some regions (including biodiversity hotspots) experiencing a ninefold increase in urban land cover over the same time period (Seto, G€ uneralp & Hutyra 2012). Accompanying the expansion of urban landscapes, it is anticipated that the human population living in cities and towns globally will increase from 3 5 to 5 billion people within the next 20 years (Fragkias et al. 2013). Thus, the demands of an expanding and urbanizing human population are one of the pressing ecological problems our world is facing (Sanderson et al. 2002), alongside, and in combination with, global climate change and changes to biodiversity at local and global scales (Pimm et al. 2014). Yet, urban environments also present a unique opportunity to expand our fundamental knowledge related to ecology and evolution due to the presence of intense and often novel selection pressures. In the inaugural issue of this journal, Calow (1987) defined functional ecology as the sum of three interactive processes: (i) those occurring between organisms and their environment, (ii) biotic interactions between organisms and (iii) adaptive processes driven by natural selection. The same three processes were highlighted 1 year earlier by Jared Diamond in Nature, when he called for biologists to pay more attention to the potential of using the unprecedented environmental conditions that exist within towns and cities to develop and test evolutionary and ecological theory (Diamond 1986). There is thus a natural synergy between functional ecology and urban ecology, as exemplified by some of the classic papers that have appeared in this journal, such as Rydell (1992) who demonstrated that the form of echolocation system determined the impact of light pollution on bat foraging behaviour. The potential of combining functional ecological research with urban ecology is, however, a long way from being fully realized. This is in part explained by the youth of urban ecology as a discipline. Scientific enquiry into the ecological consequences of urban environments has been underway for over half a century, although most of the momentum emerged after the mid 1990s (McDonnell 2011; Wu 2014). Thus, the focus of much urban research to date has involved describing patterns along environmental gradients (Gagn e 2013; McDonnell & Hahs 2013) rather than investigating the mechanistic processes that lie at the heart of functional ecology. To be effective in addressing the global challenges of urbanization, a much better understanding of how the urban environment affects the ecology and evolution of organisms needs to be developed (Grimm et al. 2008; Marzluff 2012; Gil & Brumm 2014; McDonnell & Hahs 2015). The purpose of this special feature is to draw attention to the plethora of opportunities that await researchers investigating the ecology and evolution of organisms in urban environments. The combination of environmental stressors and conditions within urban areas provides a novel opportunity to test and expand our theories related to ecology and evolution of organisms, and some intriguing insights are already beginning to emerge. For example, the detailed understanding of the molecular, genetic and developmental mechanisms of beak evolution that has arisen from studying Galapagos finches has been significantly advanced by studying beak evolution in the house finch Carpodacus mexicanus in response to novel urban food sources and its consequences for acoustic communication (Badyaev 2010, 2014). Thus, urban ecology has the potential to extend our understanding of extremely well-studied ecological and evolutionary problems.

We know little about the availability of potential prey and patterns of prey consumption by Ningaui yvonneae in a natural environment. This information is important to understanding how the species is able to exploit its semiarid environment. Here, we examine the diet of N. yvonneae inhabiting a semiarid mallee community in South Australia using a combination of faecal analysis and observations of nocturnally foraging animals. Prey consumption was compared with the availability of prey types in the environment, and comparisons made between habitat components, across seasons and between sexes. N. yvonneae was found to include a range of prey types in its diet, with 11 invertebrate taxa recorded from direct observation and eight of these detected in the scats. Prey taxa consumed most often by freely foraging ningauis were Araneae, Blattodea and Orthoptera, while those most commonly detected in scats were Hymenoptera and Araneae. In comparison, 22 invertebrate taxa were recorded in pitfall traps, although many of these were recorded infrequently. Taxa most commonly recorded in traps were Hymenoptera, Collembola, Coleoptera and Acariformes. Observational data also indicated that consumption of prey taxa differed significantly between sexes and among seasons. Males generally consumed a more diverse array of prey, with both observational and scat data showing that they were more likely to consume Hymenoptera and Isoptera, while females were more likely to consume Lepidoptera and Hemiptera. Variability between seasons was evident in consumption of invertebrate grubs (recorded only during ‘growth’; February–April), Orthoptera (recorded most often during ‘breeding’, August–October), and Araneae (recorded more often during ‘maturation’, May–July). However percentage occurrence data from the scats lacked this seasonality, possibly because of the smaller array of prey taxa recorded. N. yvonneae captured prey from all available habitat components, with five of the most frequently recorded prey taxa being recorded from all components. Leaf litter and Triodia were the most commonly recorded capture sites (45% and 22% of captures respectively), and males and females used the habitat components in a similar manner. Although N. yvonneae is like many other dasyurids in having a largely generalist insectivorous diet, comparisons of prey consumed with their availability in the environment indicated that individuals did show some selectivity towards certain taxa, particularly Blattodea, Orthoptera, Chilopoda, Lepidoptera and Araneae.

The evolution of phenotype has historically been studied by classifying traits into categories, as traits within each category often exhibit close associations. However, these categories are not independent of one another. Thus, the phenotype may function as an integrated set of traits rather than as isolated units. In this study, we employed various phylogenetic comparative methods to explore evolutionary correlations among traits, estimate and compare phylogenetic signals, and evaluate evolutionary models to assess the validity of the historical categorization of phenotypic traits in spiny lizards of the genus Sceloporus. We categorized these traits as either morphological or life-history traits, including eight morphological traits and seven life-history traits, such as trunk length, head width, snout-vent length, clutch size, hatchling length, and size at maturity. Our analyses revealed covariation in the evolution of traits both within and across categories. Differences in phylogenetic signals between categories were also observed, though these results should be interpreted with caution. Additionally, the evolutionary models varied between categories. Our findings suggest that estimates of phylogenetic signals and covariation between morphological and life-history traits are independent of historically assigned categories. Therefore, this supports the notion that traits should be compared and analyzed in an integrated manner, regardless of their category. We discuss how evolutionary mechanisms, such as fecundity selection, may influence traits across different categories (e.g., trunk length, hatchling length, and clutch size), challenging the appropriateness of traditional phenotypic categorization in evolutionary studies of Sceloporus.

Animal movement and dispersal are key factors in population dynamics and support complex ecosystem processes like cross‐boundary subsidies. Juvenile dispersal is an important mechanism for many species and often involves navigation in unfamiliar habitats. For species that metamorphose, such as amphibians, this transition from aquatic to terrestrial environments involves the growth and use of new morphological traits (e.g., legs). These traits strongly impact the fundamental ability of an organism to move in novel landscapes, but innate behaviors can regulate choices that result in the realized movements expressed. By assessing the integrative role of morphology and behavior, we can improve our understanding of juvenile movement, particularly in understudied organisms like amphibians. We assessed the roles of morphological (snout‐vent length and relative leg length) and performance (maximal jump distance) traits in shaping the free movement paths, measured through fluorescent powder tracking, in three anuran species, Pacific treefrog (Hyliola regilla), Western toad (Anaxyrus boreas), and Cascades frog (Rana cascadae). We standardized the measurement of these traits to compare the relative role of species' innate differences versus physical traits in shaping movement. Innate differences, captured by species identity, were the most significant factor influencing movement paths via total movement distance and path sinuosity. Relative leg length was an important contributor but significantly interacted with species identity. Maximal jump performance, which was significantly predicted by morphological traits, was not an important factor in movement behavior relative to species identity. The importance of species identity and associated behavioral differences in realized movement provide evidence for inherent species differences being central to the dispersal and movement of these species. This behavior may stem from niche partitioning of these sympatric species, yet it also calls into question assumptions generalizing anuran movement behavior. These species‐level effects are important in framing differences as past research is applied in management planning.

I examined sexual selection in the iguanid lizard Uta palmeri by measuring phenotypic selection in a cohort of males. Relative fitness was estimated by copulation rate from one breeding season, and I analyzed selection on five morphological traits (snout-vent length, mass, jaw length, head width, and head depth) and on male territory quality. Only territory quality and head depth were identified as direct targets of selection in a linear selection gradient analysis. Head depth was suggested to also be subject to quadratic selection. All traits exhibited significant directional selection differentials, suggesting indirect selection also was present because of the correlation of these traits with direct targets of selection. I used these results to generate hypotheses about the mechanisms of selection. For traits not identified as direct targets of selection (snout-vent length, mass, head width, jaw length), I could accept the null hypothesis of no female preference for the analyzed male traits; if these morphological traits were preferred by females in mate choice, they would have been identified as direct targets of selection. Exploring possible functional relationships within the cohort, I found that all five morphological traits contributed to explaining variation in territorial status. And in staged aggressive interactions between males that were similar in snout-vent length and mass, winning was associated only with greater head depth and not with head width or jaw length. Several possible interpretations of these results are presented. This study suggests that differential mating success arising from variation in territory quality gives rise to indirect selection on morphology. The possible mechanisms giving rise to the proposed direct selection on head depth require further study.

The effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird, Harmonia axyridis, were investigated by using a 2 × 2 factorial design in large scale cages. Prey density influenced prey consumption of the ladybirds, and the frequency with which predation occurred was quite different between the prey distributions. The ladybirds consumed a relatively constant and small number of aphids when the prey were uniformly distributed, whereas the number of prey consumed per day when predation occurred was large and much more variable when the prey were contagiously distributed. At high prey density, the number of prey consumed was highest during the first day of the experiment; thereafter, only 10–20 aphids were consumed during the following 3 days. However, these patterns of prey consumption were not observed at low prey density. The percentage of aphids that remained on the host plants when the experiments were terminated was higher at low prey density than at high prey density, suggesting that predator foraging efficiency at low prey density was lower than at high prey density. Ladybirds foraging for high prey density were more frequently observed on the plants with aphids than ladybirds foraging for low prey density. Prey distribution also influenced the frequency of residence of ladybirds on the plants. The different predation patterns observed in the two spatial distributions, in which prey consumption was much more variable for the contagious distribution, might be explained by the difference in prey encounter rate of the predator between the distributions. This study indicated that the ladybirds had limited ability to search out prey over large spatial scales.

Tropical mountains are hotspots of biodiversity and refugia for plants and animals, especially in a world of accelerating climatic change (Steinbauer et al., 2018). Biological diversity on tropical mountains is shaped by abiotic and biotic factors. Therefore, elevational gradients provide an opportunity to study effects of different ecological and evolutionary factors over relatively short geographical distances (Körner, 2007). This is a unique opportunity that inspired naturalist to use them as natural laboratories. Along elevational gradients in tropical mountains, multiple ecological questions have been explored, from diversity patterns to trait-environment relationships. Despite scientific advances in our knowledge of elevational gradients, we still lack a comprehensive understanding of numerous aspects of environmental factors and their influence on species diversity and function. In my thesis, I provide a detailed analysis to understand patterns of tropical plant diversity, particularly vascular epiphytes, and their vulnerability to anthropogenic disturbance at different spatial scales (chapter 1), and the interplay and relative importance of broad- and small-scale environmental gradients as drivers of variation in leaf functional traits of vascular epiphytes (chapter 2). Furthermore, I assembled a publicly available database of epiphyte species diversity, community composition and leaf functional traits based on data from previous chapters, with the aim of contribute and motivate future research on tropical mountains (chapter 3). In chapter 1, I analysed the response of epiphyte diversity to forest-use intensity from local to landscape scales along a tropical elevational gradient. I studied the effects of forest‐use intensity on alpha, beta, and gamma diversity of vascular epiphyte assemblages in old‐growth, degraded and secondary forests at eight study sites, yielding a total of 120 plots along the elevational gradient. I found that the interactive effects of elevation and forest‐use intensity strongly impacted local‐scale patterns of vascular epiphyte diversity. Alpha diversity did not differ significantly among forest‐use intensity levels. However, gamma diversity was always lower in secondary forests compared to old‐growth forests across the entire elevational gradient. Furthermore, beta diversity was dominated by species turnover along the forest‐use intensity gradient in the lowlands, but declined with increasing elevation, where community composition became increasingly nested. The results in this study highlight a strong interaction between forest‐use intensity and elevation. Further, this study offers a framework to better understand the ecological factors that may determine diversity patterns of epiphytes in an anthropogenic world. In chapter 2, I examined variation in morphological and chemical leaf traits of 102 vascular epiphyte species along broad- and small-scale environmental gradients, and assessed whether the variation in traits along these gradients were consistent across photosynthetic pathways (CAM and C3). I found that broad- and small-scale environmental gradients explained more variation in chemical traits than in morphological traits. For example, carbon isotope ratio (δ13C) a proxy for water-use efficiency varied systematically across both environmental gradients, suggesting a decrease of water-use efficiency with increasing elevation and an increase with relative height of attachment. Contrary to our expectations, broad- and small-scale environmental gradients explained little of the variation in morphological leaf traits, suggesting that environmental conditions do not constrain morphological leaf trait values of vascular epiphytes. Our findings suggest that analysing multiple drivers of leaf trait variation and considering photosynthetic pathways is key for disentangling functional responses of vascular epiphytes to environmental conditions. In chapter 3, I compiled a new comprehensive database (BIOVERA-Epi) that contains information on epiphyte species diversity, community composition and leaf functional traits. Moreover, I included data from 120 forest plots distributed along the studied elevational gradient which included six different forest types and three levels of forest-use intensity. In this chapter, I provided information describing two datasets in which, I assembled distribution and frequency data of 271 epiphytes species surveyed along the entire elevational gradient. Further, I measured a set of nine morphological and chemical leaf traits for 102 species surveyed along 45 plots in a section of the elevational gradient. With this chapter, I aim to contribute to future synthetic studies on the ecology, diversity, conservation, and functional plant ecology of tropical epiphyte assemblages in the Neotropics.

Editorial

Body size is known to play a critical role in determining patterns of prey selection. In this study, we examined the diets of pumpkinseed sunfish (Lepomis gibbosus) from three Michigan lakes. Pumpkinseeds have highly developed pharyngeal jaws specialized for crushing gastropods, and in our study lakes gastropods consistently contributed >80% of the prey mass in pumpkinseed diets. However, the average dietary composition and prey selection among snail taxa and size classes varied considerably among dates and sites. We hypothesized that this variation was influenced by changes in the size structure of the snail community. We used laboratory studies to quantify the effect of snail (and fish) size on three important components of the predator—prey interaction: encounter rates, attack probabilities, and capture successes. We then used these laboratory data to predict prey selection observed in the field. For most of our field situations, a simple model based on size—specific encouter rates only) explained a large percent (71%) of the observed variation in prey selection. However, in those cases where some of the snails were resistant to predation, due to crushing resistance or gape limitation, this simple model was a very poor predictor of prey selection. A more complex model (based on encounter rates and size refuges) successfully explained 46% of the variance in these cases where snails were relatively invulnerable. Finally, we compared estimates of attack probabilities with predictions from optimal foraging theory and found qualitative agreement in that fish ignored prey of low profitabilities and became more selective as the quality of the environment improved. however, the incorporation of variable attack probabilities into the foraging model resolved only a small part of the observed residual variation in selectivities because snails with low profitabilities were already underrepresented in the diet due to their low encounter rates or capture successes. This study demonstrates that predator—prey interactions in size—structured populations can create apparently complex variation in prey selection, but that this variation can be largely understood within a framework that simultaneously considers the dynamics of prey size distributions and how components of the foraging interaction scale with body size of the predator and prey.

Cheliped morphological variation of the intertidal crab Eriphia verrucosa across shores of differing exposure to wave action

Aspects of the reproductive biology of a trogloxene population of the pickerel frog, Rana palustris (Anura: Ranidae), were studied at a cave on the edge of the Ozark plateau in Missouri. Sexual dimorphism in body size was marked; there was almost no overlap in adult body size ranges, and the ratio of mean adult female snout–vent length (SVL) to adult male SVL was 1.26. All males with SVL of >45 mm were sexually mature. Males showed a clear cycle of spermatogenesis, with a peak in midsummer and a decline in spermatogenic activity through autumn and winter. Minimum size at maturity for females was 59 mm SVL. Females completed vitellogenesis during the summer, before their arrival at the study site. Of 28 females above the minimum size at maturity, 27 contained egg clutches. Clutch size, clutch mass, and egg size (mass) show significant positive correlation with SVL. Mean (±SD) clutch size was 1759 ± 548. Fat bodies were present in both males and females in autumn, but were totally depleted before the animals emerged from hibernation. Trogloxene R. palustris do not diverge significantly from patterns of reproductive biology typical of other temperate zone Rana. Current or past patterns of cave use have had no detectable effect on reproductive characteristics of trogloxene R. palustris.

Changes in morphological traits, such as body size, body condition, and leg length, are important indicators of changes to life history or habitat quality, which can affect the performance of individuals and therefore the persistence of populations under environmental change. Only very few studies assessed the effect of fragmentation on morphological traits. The few available studies on anurans found that in landscapes with less forest cover body size decreased. Therefore, we predict that body size should also be smaller in fragments compared to continuous forest. Body condition is a further trait closely related to individual performance and thus should decline with more adverse conditions, as is expected in fragments. We tested these hypotheses using snout-vent length, body mass, body condition, and tibia length as response variables. We collected data of a habitat generalist (Rhinella ornata) and a habitat specialist (Ischnocnema guentheri), both leaf-litter amphibian species, from three sites in a fragmented landscape (two isolated and one connected site) and one site in a contiguous part of the Atlantic Forest of Southeast Brazil. In the generalist species, snout-vent-length (SVL) and body mass were significantly lower in fragments compared to the contiguous forest control, whereas tibia length and body condition did not differ among sites. In contrast, SVL, body mass, and tibia length of the specialist species did not differ among sites, but body condition was marginally different among sites, being relatively low in one but not the other isolated fragment. The results indicate that different processes affect the morphology of the two species following habitat fragmentation.

In animals with a complex life cycle, changes in biotic and abiotic conditions during development can alter growth and maturation rates, causing carry-over effects in postmetamorphic phenotypes. In anurans, this developmental plasticity can result in a trade-off between length of larval period and body size at metamorphosis in stressful environments. Secondary salinisation has been identified as a substantial stressor to amphibians; however, little is known about how salinity-induced developmental plasticity differs between anuran populations. We examined differences in survival, time to metamorphosis, size at metamorphosis (mass and snout–vent length) and body condition at metamorphosis in response to elevated salinity in three populations of the brown tree frog (Litoria ewingii). Significant differences in size at metamorphosis between salinity treatments were observed in tadpoles sourced from freshwater wetlands and ephemeral wetlands, with tadpoles showing a reduced mass and snout–vent length at metamorphosis in the higher-salinity treatment. There were no significant differences in metamorphic traits between salinity treatments in tadpoles sourced from a consistently brackish wetland, suggesting either an erosion of developmental plasticity in response to elevated salinity, or the magnitude of salinity required to alter developmental traits is higher in this population. Our results indicate that environmental conditions of source populations need to be considered when studying life-history adaptations in response to environmental change.

Chapter 6 - Nutrient cycling

Simple SummaryAmphibians have weak dispersal abilities and are sensitive to environmental changes, resulting in their disproportionately high risk of extinction, with many species’ populations rapidly declining. Therefore, it is critical for amphibian conservation to understand their adaptive potential by exploring how amphibians respond to environmental changes based on morphological variations. Our results showed that morphological traits of Feirana taihangnica significantly differed among ages. Along with the increase in annual mean temperature, snout-vent length showed an anti-hump trend, indicating no support for Bergmann’s rule. Mean ultraviolet-B of the highest and lowest months were positively and negatively correlated with head width, thigh length and tibia width, respectively. The present study can help understand the effects of environmental changes on morphological variations of this mountain frog species and its adaptive potential, providing important implications for species conservation.The Taihangshan swelled-vented frog (Feirana taihangnica), an endemic species to the Qinling Mountains, central China, has experienced a dramatic population decline over the last few decades. The aim of this work was to quantify morphological variation in F. taihangnica across the Qinling Mountains and examine environmental correlates of this variation of morphological traits. We implemented a hierarchical partitioning to estimate the independent contribution of each environmental variable on morphological variations. Temperature seasonality was the greatest contributor in variations of snout-vent length (SVL) and head width, and ultraviolet-B (UV-B) radiation of the lowest month was the most influential on both thigh length and tibia width. Then, we used generalized additive models to analyze the relationship between each environmental factor and morphological trait variations. Along the increasing of annual mean temperature, SVL decreased firstly and then increased, indicating no support for Bergmann’s rule. Furthermore, SVL was negatively correlated with annual precipitation, while positively with temperature seasonality. The mean UV-B of the highest and lowest months was positively and negatively correlated with head width, thigh length and tibia width, respectively. The results of this study help us to understand adaptive potential of this mountain frog species via morphological variations in the light of environmental changes.