Niche overlap in rodents increases with competition but not ecological opportunity: A role of inter-individual difference.

Niche variation at population level mediates niche packing (i.e. patterns of species' spread within the niche space) and species coexistence at community level. Competition and ecological opportunity (resource diversity) are two of the main mechanisms underlying niche variation. Dense niche packing could occur through increased niche partitioning or increased niche overlap. In this study, we used stable carbon and nitrogen isotope data of 635 individual rodents from four species across nine sites in the montane region of a subtropical island to test the effects of competition and ecological opportunity on population isotope niche size, inter-individual niche difference within population and interspecific niche overlap within community. We used the Bayesian Standard Ellipse Area (SEAB, the ellipse area enclosed by carbon and nitrogen isotope values of organisms on a bi-plot) to estimate population niche size and interspecific niche overlap. Inter-individual niche difference within population was quantified as isotopic divergence and isotopic uniqueness. We used rodent abundance (the number of unique individuals captured) to measure competition and plant isotope niche size (plant SEAB) to measure ecological opportunity. The rodents experienced competition as evidenced by a negative relationship between population change rate and conspecific abundance. Rodent population niche size increased with ecological opportunity but not competition. The inter-individual niche difference (isotopic uniqueness) increased with competition (interspecific competition only) but not ecological opportunity. At community level, interspecific niche overlap (herbivore-omnivore pair only) increased with competition (the combined abundance of the pair) but not ecological opportunity. This study demonstrated that isotope niche variation of the rodents could be hierarchically influenced by ecological opportunity and competition, with the former setting the limit of population niche size across communities and the latter shaping inter-individual niche difference and interspecific niche overlap within communities. Under strong intraspecific competition and limited ecological opportunity for niche expansion, individuals may choose to increase their isotopic uniqueness from conspecifics at the cost of overlapping with heterospecifics of different trophic roles within the community niche space as overall competition increases. Denser niche packing of these rodent communities might be achieved through increased niche overlap.

Niche-trait relationships at individual and population level in three co-occurring passerine species.

The niche variation hypothesis (NVH) predicts that populations with wider niches exhibit greater morphological variation through increased interindividual differences in both niche and morphology. In this study, we examined niche-trait relationships in three passerine species (Cyanoderma ruficeps, Sinosuthora webbiana, and Zosterops simplex). A total of 289 C. ruficeps from 7 sites, 259 S. webbiana from 8 sites, and 144 Z. simplex from 6 sites were sampled along an elevation gradient (0-2,700 m) in Taiwan from 2009 to 2017. We measured bill traits (length, width, and depth of bill) and body size traits (length of head, tarsus, and wing) of the birds, which were reduced to four principal components (bill PC1, bill PC2, body size PC1, and body size PC2). We collected feather tissues for stable carbon and nitrogen isotope analyses to quantify their isotope niche. We quantified interindividual differences in isotope space and trait space with four diversity metrics (divergence, dispersion, evenness, and uniqueness) and tested whether interindividual differences in isotope space and trait space are positively associated. We quantified population isotope niche width by Bayesian ellipse area and population morphological variation by variances of the PCs. The results showed that individual uniqueness in isotope niche and bill morphology (average closeness of individuals within the population isotope/trait space) were positively associated across three species. Furthermore, isotope niche width and bill PC1 (reflecting the size of bill) variation at population level were also positively associated across the three species, supporting the NVH. Of the three species, C. ruficeps and S. webbiana showed stronger support for the NVH than Z. simplex, possibly due to the latter having narrower elevational distribution and a more specialized, plant-based diet. The diversity metrics represented different aspects of interindividual differences in niche/trait space, and for the passerines, individual uniqueness appeared to play an important role in their niche-trait dynamics.

Long-term monitoring reveals invariant clutch size and unequal reproductive costs between sexes in a subtropical lacertid lizard.

Based on 20,000 records representing c. 11,000 individuals from an 8-year capture-mark-recapture (CMR) study, we tested and confirmed a new case of invariant clutch size (ICS) in a sexually dichromatic lacertid lizard, Takydromus viridipunctatus. In the grassland habitat of the early succession stage, females showed strictly low and invariant clutch size, multiple clutches in a breeding season, high reproductive potential, and annual breeding cycles that correspond to the emergence of male courtship coloration. The hatchlings mature quickly, and join the adult cohort for breeding within a few months, whereas adults show low survival rates and a short lifespan, such that most die within one year. Mortality increased in both sexes during the breeding season, especially in females, indicating an unequal cost of reproduction in survival. These life history characters may be explained by two non-exclusive hypotheses of ICS-arboreal hypothesis and predation hypothesis-within the ecological context of their habitat. Our study highlights a confirmed case of ICS, which adapts well to this r-selected grassland habitat that experiences seasonal fluctuation and frequent disturbance.

When males live longer: Resource-driven territorial behavior drives sex-specific survival in snakes.

Phylogenetic analysis has shown that males' propensity to engage in aggressive encounters is associated with females having greater longevity. Here, we confirm the causal link between aggression and reduced longevity by looking at an egg-eating snake (Oligodon formosanus) in which females defend territories in the presence of sea turtle eggs. We monitored aggressiveness and survival at two sites: a control site with a stable supply of turtle eggs, and a second site where we collected data before and after a storm that eroded the beach on which turtles nested, thus leading to a loss of territoriality. We show that territoriality was the driver behind higher injury rates in females. Territorial females also had lower survival and decreased longevity compared with the nonterritorial males, but these differences disappeared when females were not territorial. Our study demonstrates how resource availability can influence the evolution of sex-specific patterns of survival across vertebrates.

The effects of food and parasitism on reproductive performance of a wild rodent.

Food and parasitism can have complex effects on small mammal reproduction. In this study, we tested the effects of sex, food, and parasitism on reproductive performance of the Taiwan field mouse (Apodemus semotus). In a field experiment, we increased food availability for a portion of the mice in the population by providing sorghum seeds to a set of food stations. We reduced parasite intensity of randomly chosen mice through ivermectin treatment. We determined the number and quality of offspring for the mice using paternity analysis. We quantified seed consumption with stable carbon isotope values of mouse plasma and parasite intensity with fecal egg counts of intestinal nematodes and cestodes (FEC). In a laboratory experiment, we reduced parasite intensity of randomly chosen mice through ivermectin treatment. We quantified their immune functions by total white blood cell count, percent granulocyte count, and percent lymphocyte count through hematological analyses. We measured the FEC and energy intake of the mice. From the field experiment, the number of offspring in A. semotus increased with increasing seed consumption. Due to the trade-off between number and quality of offspring, the offspring quality decreased with increasing seed consumption for the females. The ivermectin treatment did not affect offspring number or quality. However, the FEC was positively correlated with number of offspring. In the laboratory experiment, the percent lymphocyte/granulocyte count changed with parasite intensity at low energy intake, which was relaxed at high energy intake. This study demonstrated positive effects of food availability and neutral effects of parasitism on A. semotus reproduction. However, the benefits of food availability for the females need to take into account the offspring number-quality trade-off, and at high infection intensity, parasitism might negatively affect offspring quality for the males. We suggest that food availability could mediate the relationships between parasite intensity and immune responses.

Effects of Greenfall on Ground-dwelling Arthropods in a Subtropical Forest.

Chien-Lung Chen and Pei-Jen L. Shaner (2018) Resource events such as typhoon-triggered greenfall have consequences for multiple ecological mechanisms, ranging from population dynamics and trophic interactions to ecosystem processes. Arthropods are sensitive to environmental disturbances, and many taxa have been used as indicator species. In a field experiment, we tested the effects of greenfall on ground-dwelling arthropods (mostly litter-dwelling taxa) in a forest of Taiwan red pine (Pinus taiwanensis) in the summer of 2013. Of 20 field plots (5 × 5 m), half received P. taiwanensis greenfall while the other half served as unaltered controls. As predicted, some arthropod taxa responded more strongly than others to the greenfall addition. Among the examined arthropod taxa (Araneae, Coleoptera: Carabidae, Coleoptera: Staphylinidae, Hymenoptera: Formicidae, Collembola, Isopoda: Oniscidea), the predatory staphylid beetles (Staphylinidae) responded positively to greenfall addition while the larger-sized detritivore woodlice (Oniscidea) responded negatively. Contrary to our prediction of a positive response, the smaller-sized detritivore springtails (Collembola) were unaffected by the greenfall addition. At the beginning of this study, we observed short-term effects of a naturally- occurring typhoon, to which springtails and ants (Formicidae) responded negatively while staphylid beetles responded positively. Also contrary to our prediction, these taxon-specific responses did not suffice to alter the composition of arthropod communities. We concluded that the intra-annual effects of typhoons-specifically those associated with greenfall-are more likely to impact certain taxa, including staphylid beetles, woodlice, springtails and ants. At the taxonomic level examined here, these intra-annual effects on community composition are non-detectable. As typhoon frequency and intensity are likely to change with global warming, the study makes a timely contribution to our understanding of typhoon-induced ecological dynamics in subtropical plantation forests.

Corrigendum: Developing informative microsatellite markers for non-model species using reference mapping against a model species' genome.

This corrects the article DOI: 10.1038/srep23087.

Geographic variation in advertisement calls of a Microhylid frog - testing the role of drift and ecology.

Acoustic signals for mating are important traits that could drive population differentiation and speciation. Ecology may play a role in acoustic divergence through direct selection (e.g., local adaptation to abiotic environment), constraint of correlated traits (e.g., acoustic traits linked to another trait under selection), and/or interspecific competition (e.g., character displacement). However, genetic drift alone can also drive acoustic divergence. It is not always easy to differentiate the role of ecology versus drift in acoustic divergence. In this study, we tested the role of ecology and drift in shaping geographic variation in the advertisement calls of Microhyla fissipes. We examined three predictions based on ecological processes: (1) the correlation between temperature and call properties across M. fissipes populations; (2) the correlation between call properties and body size across M. fissipes populations; and (3) reproductive character displacement (RCD) in call properties between M. fissipes populations that are sympatric with and allopatric to a congener M. heymonsi. To test genetic drift, we examined correlations among call divergence, geographic distance, and genetic distance across M. fissipes populations. We recorded the advertisement calls from 11 populations of M. fissipes in Taiwan, five of which are sympatrically distributed with M. heymonsi. We found geographic variation in both temporal and spectral properties of the advertisement calls of M. fissipes. However, the call properties were not correlated with local temperature or the callers' body size. Furthermore, we did not detect RCD. By contrast, call divergence, geographic distance, and genetic distance between M. fissipes populations were all positively correlated. The comparisons between phenotypic Q st (P st) and F st values did not show significant differences, suggesting a role of drift. We concluded that genetic drift, rather than ecological processes, is the more likely driver for the geographic variation in the advertisement calls of M. fissipes.

Developing informative microsatellite markers for non-model species using reference mapping against a model species' genome.

Microsatellites have a wide range of applications from behavioral biology, evolution, to agriculture-based breeding programs. The recent progress in the next-generation sequencing technologies and the rapidly increasing number of published genomes may greatly enhance the current applications of microsatellites by turning them from anonymous to informative markers. Here we developed an approach to anchor microsatellite markers of any target species in a genome of a related model species, through which the genomic locations of the markers, along with any functional genes potentially linked to them, can be revealed. We mapped the shotgun sequence reads of a non-model rodent species Apodemus semotus against the genome of a model species, Mus musculus, and presented 24 polymorphic microsatellite markers with detailed background information for A. semotus in this study. The developed markers can be used in other rodent species, especially those that are closely related to A. semotus or M. musculus. Compared to the traditional approaches based on DNA cloning, our approach is likely to yield more loci for the same cost. This study is a timely demonstration of how a research team can efficiently generate informative (neutral or function-associated) microsatellite markers for their study species and unique biological questions.

Trophic cascade effects of avian predation on a willow in an urban wetland.

Trophic cascades play a crucial role in ecosystem functioning. In this study, we tested the effects of avian predation on willows (Salix warburgii) and associated arthropods in an urban wetland. We excluded birds by netting around willow branches for 20 months from September-November 2010 to June 2012. We compared the leaf count, leaf area, leaf biomass, bud count, catkin (flower) count and herbivory from pairs of bird-exclusion and no-exclusion branches on 11 trees. Simultaneously, we compared herbivorous and predatory arthropod abundances associated with bird-exclusion and no-exclusion branches. Another nine trees were used as reference branches to assess whether the bird exclusion impacted other branches of the same trees (i.e., no-exclusion branches). Bird exclusion resulted in increased herbivory 1 year after the treatment, followed by a reduced leaf count, leaf area, leaf biomass, bud count and catkin count in the second year. The bird-exclusion branches exhibited greater spider abundance than the no-exclusion branches. However, herbivorous arthropod abundances were similar between the branch types. The reference branches had similar values in all plant traits and for all arthropod abundances to those of the no-exclusion branches. This study demonstrated the branch-level effects of trophic cascades on willows via the exclusion of birds and a resulting reduction in herbivory. However, whether and how the arthropods mediate such effects require further investigation. This study adds to the limited empirical data demonstrating the effects of trophic cascades on plant reproduction. Our findings highlight the importance of bird conservation in urban wetlands.

Climate niche differentiation between two passerines despite ongoing gene flow.

Niche evolution underpins the generation and maintenance of biological diversity, but niche conservatism, in which niches remain little changed over time in closely related taxa, and the role of ecology in niche evolution are continually debated. To test whether climate niches are conserved in two closely related passerines in East Asia - the vinous-throated (Paradoxornis webbianus) and ashy-throated (P. alphonsianus) parrotbills - we established their potential allopatric and sympatric regions using ecological niche models and compared differences in their climate niches using niche overlap indices in background tests and multivariate statistical analyses. We also used polymorphism data on 44 nuclear genes to infer their divergence demography. We found that these two parrotbills occupy different climate niches, in both their allopatric and potential sympatric regions. Because the potential sympatric region is the area predicted to be suitable for both parrotbills based on the ecological niche models, it can serve as a natural common garden. Therefore, their observed niche differences in this potential sympatry were not simply rendered by phenotypic plasticity and probably had a genetic basis. Our genetic analyses revealed that the two parrotbills are not evolutionarily independent for the most recent part of their divergence history. The two parrotbills diverged c. 856,000 years ago and have had substantial gene flow since a presumed secondary contact c. 290,000 years ago. This study provides an empirical case demonstrating that climate niches may not be homogenized in nascent species in spite of substantial, ongoing gene flow, which in turn suggests a role for ecology in promoting and maintaining diversification among incipient species.

Sex-specific effects of parasitism on survival and reproduction of a rodent host in a subtropical montane region.

Parasites can generate complex life history trade-offs in a host. In this study, we experimentally reduced the infection level of intestinal helminth parasites in the Taiwan field mouse (Apodemus semotus) to test (1) whether parasite richness and load are biased towards male or female mice (sex-biased parasitism) and (2) whether the effects of parasitism on the host's survival and reproduction are different between the sexes (sex-specific effects of parasitism). Our findings indicate that neither parasite richness (number of helminth taxa found in a fecal sample) nor parasite load (number of helminth eggs per gram of fecal material) was sexually biased in our A. semotus study population. These results are in agreement with those of previous studies on endoparasites in Apodemus spp., but are in contrast to those on ectoparasites in Apodemus spp. Parasite removal reduced the survival rate of reproducing females, possibly by allowing reproducing females to increase maternal investment in their current litters at the cost of their own future survival. Single-litter mothers with reduced parasitism had a higher body mass than the untreated single-litter mothers, suggesting an increased maternal investment. In addition, the reproductively more active A. semotus, particularly the females, carried higher parasite loads, suggesting a trade-off between reproduction and parasite defense. By demonstrating that parasites can affect life history trade-offs in A. semotus, our results highlight the importance of maintaining variation in life history traits under parasitism risks and illustrate the subtle demographic processes (e.g. reduced future survival among healthy reproducing females) that might be driven by parasitism.

Drastic population fluctuations explain the rapid extinction of the passenger pigeon.

To assess the role of human disturbances in species' extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3-5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon's extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon's effective population size throughout the last million years was persistently about 1/10,000 of the 1800's estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an "outbreak" species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial-interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon's rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history.

Sex-specific correlations of individual heterozygosity, parasite load, and scalation asymmetry in a sexually dichromatic lizard.

Heterozygosity-fitness correlations (HFCs) provide insights into the genetic bases of individual fitness variation in natural populations. However, despite decades of study, the biological significance of HFCs is still under debate. In this study, we investigated HFCs in a large population of the sexually dimorphic lizard Takydromus viridipunctatus (Lacertidae). Because of the high prevalence of parasitism from trombiculid mites in this lizard, we expect individual fitness (i.e., survival) to decrease with increasing parasite load. Furthermore, because morphological asymmetry is likely to influence individuals' mobility (i.e., limb asymmetry) and male biting ability during copulation (i.e., head asymmetry) in this species, we also hypothesize that individual fitness should decrease with increasing morphological asymmetry. Although we did not formally test the relationship between morphological asymmetry and fitness in this lizard, we demonstrated that survival decreased with increasing parasite load using a capture-mark-recapture data set. We used a separate sample of 140 lizards to test the correlations between individual heterozygosity (i.e., standardized mean d(2) and HL based on 10 microsatellite loci) and the two fitness traits (i.e., parasite load and morphological asymmetry). We also evaluated and excluded the possibility that single-locus effects produced spurious HFCs. Our results suggest male-only, negative correlations between individual heterozygosity and parasite load and between individual heterozygosity and asymmetry, suggesting sex-specific, positive HFCs. Male T. viridipunctatus with higher heterozygosity tend to have lower parasite loads (i.e., higher survival) and lower asymmetry, providing a rare example of HFC in reptiles.

Trophic shifts of a generalist consumer in response to resource pulses.

Trophic shifts of generalist consumers can have broad food-web and biodiversity consequences through altered trophic flows and vertical diversity. Previous studies have used trophic shifts as indicators of food-web responses to perturbations, such as species invasion, and spatial or temporal subsidies. Resource pulses, as a form of temporal subsidies, have been found to be quite common among various ecosystems, affecting organisms at multiple trophic levels. Although diet switching of generalist consumers in response to resource pulses is well documented, few studies have examined if the switch involves trophic shifts, and if so, the directions and magnitudes of the shifts. In this study, we used stable carbon and nitrogen isotopes with a Bayesian multi-source mixing model to estimate proportional contributions of three trophic groups (i.e. producer, consumer, and fungus-detritivore) to the diets of the White-footed mouse (Peromyscus leucopus) receiving an artificial seed pulse or a naturally-occurring cicadas pulse. Our results demonstrated that resource pulses can drive trophic shifts in the mice. Specifically, the producer contribution to the mouse diets was increased by 32% with the seed pulse at both sites examined. The consumer contribution to the mouse diets was also increased by 29% with the cicadas pulse in one of the two grids examined. However, the pattern was reversed in the second grid, with a 13% decrease in the consumer contribution with the cicadas pulse. These findings suggest that generalist consumers may play different functional roles in food webs under perturbations of resource pulses. This study provides one of the few highly quantitative descriptions on dietary and trophic shifts of a key consumer in forest food webs, which may help future studies to form specific predictions on changes in trophic interactions following resource pulses.