Disentangling the effects of plant species invasion and urban development on arthropod community composition.

Urban development and species invasion are two major global threats to biodiversity. These threats often co-occur, as developed areas are more prone to species invasion. However, few empirical studies have tested if both factors affect biodiversity in similar ways. Here we study the individual and combined effects of urban development and plant invasion on the composition of arthropod communities. We assessed 36 paired invaded and non-invaded sample plots, invaded by the plant Antigonon leptopus, with half of these pairs located in natural and the other half in developed land-use types on the Caribbean island of St. Eustatius. We used several taxonomic and functional variables to describe community composition and diversity. Our results show that both urban development and A. leptopus invasion affected community composition, albeit in different ways. Development significantly increased species richness and exponential Shannon diversity, while invasion had no effect on these variables. However, invasion significantly increased arthropod abundance and caused biotic homogenization. Specifically, uninvaded arthropod communities were distinctly different in species composition between developed and natural sites, while they became undistinguishable after A. leptopus invasion. Moreover, functional variables were significantly affected by species invasion, but not by urban development. Invaded communities had higher community-weighted mean body size and the feeding guild composition of invaded arthropod communities was characterized by the exceptional numbers of nectarivores, herbivores, and detritivores. With the exception of species richness and exponential Shannon diversity, invasion influenced four out of six response variables to a greater degree than urban development did. Hence, we can conclude that species invasion is not just a passenger of urban development but also a driver of change.

Evolutionary time drives global tetrapod diversity.

Global variation in species richness is widely recognized, but the explanation for what drives it continues to be debated. Previous efforts have focused on a subset of potential drivers, including evolutionary rate, evolutionary time (maximum clade age of species restricted to a region), dispersal (migration from one region to another), ecological factors and climatic stability. However, no study has evaluated these competing hypotheses simultaneously at a broad spatial scale. Here, we examine their relative contribution in determining the richness of the most comprehensive dataset of tetrapods to our knowledge (84% of the described species), distinguishing between the direct influences of evolutionary rate, evolutionary time and dispersal, and the indirect influences of ecological factors and climatic stability through their effect on direct factors. We found that evolutionary time exerted a primary influence on species richness, with evolutionary rate being of secondary importance. By contrast, dispersal did not significantly affect richness patterns. Ecological and climatic stability factors influenced species richness indirectly by modifying evolutionary time (i.e. persistence time) and rate. Overall, our findings suggest that global heterogeneity in tetrapod richness is explained primarily by the length of time species have had to diversify.

Human land use promotes the abundance and diversity of exotic species on Caribbean islands.

Human land use causes major changes in species abundance and composition, yet native and exotic species can exhibit different responses to land use change. Native populations generally decline in human-impacted habitats while exotic species often benefit. In this study, we assessed the effects of human land use on exotic and native reptile diversity, including functional diversity, which relates to the range of habitat use strategies in biotic communities. We surveyed 114 reptile communities from localities that varied in habitat structure and human impact level on two Caribbean islands, and calculated species richness, overall abundance, and evenness for every plot. Functional diversity indices were calculated using published trait data, which enabled us to detect signs of trait filtering associated with impacted habitats. Our results show that environmental variation among sampling plots was explained by two Principal Component Analysis (PCA) ordination axes related to habitat structure (i.e., forest or nonforest) and human impact level (i.e., addition of man-made constructions such as roads and buildings). Several diversity indices were significantly correlated with the two PCA axes, but exotic and native species showed opposing responses. Native species reached the highest abundance in forests, while exotic species were absent in this habitat. Human impact was associated with an increase in exotic abundance and species richness, while native species showed no significant associations. Functional diversity was highest in nonforested environments on both islands, and further increased on St. Martin with the establishment of functionally unique exotic species in nonforested habitat. Habitat structure, rather than human impact, proved to be an important agent for environmental filtering of traits, causing divergent functional trait values across forested and nonforested environments. Our results illustrate the importance of considering various elements of land use when studying its impact on species diversity and the establishment and spread of exotic species.

Benefits and limitations of three-dimensional printing technology for ecological research.

BACKGROUND: Ecological research often involves sampling and manipulating non-model organisms that reside in heterogeneous environments. As such, ecologists often adapt techniques and ideas from industry and other scientific fields to design and build equipment, tools, and experimental contraptions custom-made for the ecological systems under study. Three-dimensional (3D) printing provides a way to rapidly produce identical and novel objects that could be used in ecological studies, yet ecologists have been slow to adopt this new technology. Here, we provide ecologists with an introduction to 3D printing. RESULTS: First, we give an overview of the ecological research areas in which 3D printing is predicted to be the most impactful and review current studies that have already used 3D printed objects. We then outline a methodological workflow for integrating 3D printing into an ecological research program and give a detailed example of a successful implementation of our 3D printing workflow for 3D printed models of the brown anole, Anolis sagrei, for a field predation study. After testing two print media in the field, we show that the models printed from the less expensive and more sustainable material (blend of 70% plastic and 30% recycled wood fiber) were just as durable and had equal predator attack rates as the more expensive material (100% virgin plastic). CONCLUSIONS: Overall, 3D printing can provide time and cost savings to ecologists, and with recent advances in less toxic, biodegradable, and recyclable print materials, ecologists can choose to minimize social and environmental impacts associated with 3D printing. The main hurdles for implementing 3D printing-availability of resources like printers, scanners, and software, as well as reaching proficiency in using 3D image software-may be easier to overcome at institutions with digital imaging centers run by knowledgeable staff. As with any new technology, the benefits of 3D printing are specific to a particular project, and ecologists must consider the investments of developing usable 3D materials for research versus other methods of generating those materials.

Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance.

The root microbiome is composed of an incredibly diverse microbial community that provides services to the plant. A major question in rhizosphere research is how species in root microbiome communities interact with each other and their host. In the nutrient mutualism between host plants and arbuscular mycorrhizal fungi (AMF), competition often leads to certain species dominating host colonization, with the outcome being dependent on environmental conditions. In the past, it has been difficult to quantify the abundance of closely related species and track competitive interactions in different regions of the rhizosphere, specifically within and outside the host. Here, we used an artificial root system (in vitro root organ cultures) to investigate intraradical (within the root) and extraradical (outside the root) competitive interactions between two closely related AMF species, Rhizophagus irregularis and Glomus aggregatum, under different phosphorus availabilities. We found that competitive interactions between AMF species reduced overall fungal abundance. R. irregularis was consistently the most abundant symbiont for both intraradical and extraradical colonization. Competition was the most intense for resources within the host, where both species negatively affected each other's abundance. We found the investment ratio (i.e. extraradical abundance/intraradical abundance) shifted for both species depending on whether competitors were present or not. Phosphorus availability did not change the outcome of these interactions. Our results suggest that studies on competitive interactions should focus on intraradical colonization dynamics and consider how changes in investment ratio are mediated by fungal species interactions.

Multilevel statistical models and the analysis of experimental data.

Data sets from ecological experiments can be difficult to analyze, due to lack of independence of experimental units and complex variance structures. In addition, information of interest may lie in complicated contrasts among treatments, rather than direct output from statistical tests. Here, we present a statistical framework for analyzing data sets containing non-independent experimental units and differences in variance among treatments (heteroscedasticity) and apply this framework to experimental data on interspecific competition among three tadpole species. Our framework involves three steps: (1) use a multilevel regression model to calculate coefficients of treatment effects on response variables; (2) combine coefficients to quantify the strength of competition (the target information of our experiment); and (3) use parametric bootstrapping to calculate significance of competition strengths. We repeated this framework using three multilevel regression models to analyze data at the level of individual tadpoles, at the replicate level, and at the replicate level accounting for heteroscedasticity. Comparing results shows the need to correctly specify the statistical model, with the model that accurately accounts for heteroscedasticity leading to different conclusions from the other two models. This approach gives a single, comprehensive analysis of experimental data that can be used to extract informative biological parameters in a statistically rigorous way.

Multiple paternity in the invasive spotted lanternfly (Hemiptera: Fulgoridae).

In biological invasions, multiple paternity can preserve genetic diversity over time and space and contribute to invasion success. Therefore, knowledge on the mating system of invasive species is essential to develop adequate management practices to mitigate their impact on ecosystems. The spotted lanternfly, Lycorma delicatula (White, 1845), is an invasive pest that has colonized more than 10 eastern US states in less than 10 yr. Multiple paternity may contribute to its success, but little is known about spotted lanternfly's mating system. We explored the mating system using mated females and female-egg mass pairs sampled in the field. First, we assessed the existence of multiple mating by counting the number of spermatophores in the genital tract of all females. Second, we searched for genetic evidence for multiple paternity within egg masses by genotyping the female-egg mass pairs at 7 microsatellite loci. Third, we assessed whether multiple mating was correlated with female traits and distance from the introduction site. One to 3 spermatophores per female were found during dissections, confirming the existence of polyandrous female spotted lanternfly. We found genetic evidence for a minimum of 2 fathers in 4 egg masses associated with polyandrous females, validating multiple paternity in spotted lanternfly. Multiple paternity was associated with egg mass size, and multiple paternity was highest in populations closest to the original introduction site and decreased toward the invasion front. Multiple paternity may contribute to the invasion success of spotted lanternfly, and control efforts should consider the mating system and the implications of its spatial patterns.

Spotted! Computer-aided individual photo-identification allows for mark-recapture of invasive spotted lanternfly (Lycorma delicatula).

The spotted lanternfly is an invasive pest for which we lack individual movement data due in part to the difficulty posed by individual identification. We developed a computer-aided method to identify individual adult spotted lanternfly using wing spot patterns from photos processed in the software I3S and demonstrated the method's accuracy with lab and field validations. Based on 176 individuals in the lab, we showed that digitizing the spots of one wing allowed a 100% reliable individual identification. The errors due to user input and the variation in the angle of the image were largely negligible compared to inter-individual variations. We applied this method in the context of a mark-recapture experiment to assess the feasibility of this method in the field. We initially identified a total of 84 unique spotted lanternflies, 31 of which were recaptured after four hours along with 49 new individuals. We established that the analysis of recaptures can possibly be automated based on scores and may not require systematic visual pairwise comparison. The demonstration of the effectiveness of this method on relatively small sample sizes makes it a promising tool for field experimentation as well as lab manipulations. Once validated on larger datasets and in different contexts, it will provide ample opportunity to collect useful data on spotted lanternfly ecology that can greatly inform management.

Paninvasion severity assessment of a U.S. grape pest to disrupt the global wine market.

Economic impacts from plant pests are often felt at the regional scale, yet some impacts expand to the global scale through the alignment of a pest's invasion potentials. Such globally invasive species (i.e., paninvasives) are like the human pathogens that cause pandemics. Like pandemics, assessing paninvasion risk for an emerging regional pest is key for stakeholders to take early actions that avoid market disruption. Here, we develop the paninvasion severity assessment framework and use it to assess a rapidly spreading regional U.S. grape pest, the spotted lanternfly planthopper (Lycorma delicatula; SLF), to spread and disrupt the global wine market. We found that SLF invasion potentials are aligned globally because important viticultural regions with suitable environments for SLF establishment also heavily trade with invaded U.S. states. If the U.S. acts as an invasive bridgehead, Italy, France, Spain, and other important wine exporters are likely to experience the next SLF introductions. Risk to the global wine market is high unless stakeholders work to reduce SLF invasion potentials in the U.S. and globally.

Understanding global and regional patterns of termite diversity and regional functional traits.

Our understanding of broad-scale biodiversity and functional trait patterns is largely based on plants, and relatively little information is available on soil arthropods. Here, we investigated the distribution of termite diversity globally and morphological traits and diversity across China. Our analyses showed increasing termite species richness with decreasing latitude at both the globally, and within-China. In addition, we detected obvious latitudinal trends in the mean community value of termite morphological traits on average, with body size and leg length decreasing with increasing latitude. Furthermore, temperature, NDVI and water variables were the most important drivers controlling the variation in termite richness, and temperature and soil properties were key drivers of the geographic distribution of termite morphological traits. Our global termite richness map is one of the first high resolution maps for any arthropod group and especially given the functional importance of termites, our work provides a useful baseline for further ecological analysis.

Breakdown in postmating isolation and the collapse of a species pair through hybridization.

Species that evolved through ecological speciation and that lack intrinsic genetic incompatibilities may nonetheless be maintained by extrinsic postmating isolating barriers that impose selection against hybrids. These species, however, may be vulnerable to a breakdown in postmating isolation. Here, we investigate a model system for ecological speciation: sympatric limnetic-benthic pairs of threespine sticklebacks. Recently, stickleback hybrid abundance in Enos Lake has increased. Given that ecological selection against hybrids was historically an important component of total reproductive isolation, we tested whether ecologically dependent postmating isolation is still functioning. We compared body shape, diet, growth, and survival in present-day Enos fish with trait data in the undisturbed Paxton Lake species pair and with historical Enos Lake data. In both Paxton and historical Enos data, we found a strong correlation between body shape and diet; however, in present-day Enos fish, this correlation was absent. Using fitness estimates based on growth rates and survival, we found no evidence of selection against intermediate morphologies. It appears that postmating isolation has broken down, allowing hybrids to persist and contributing to the collapse of the species pair.

Species diversity as a surrogate for conservation of phylogenetic and functional diversity in terrestrial vertebrates across the Americas.

Preserving the evolutionary history and ecological functions that different species embody, in addition to species themselves, is a growing concern for conservation. Recent studies warn that conservation priority regions identified using species diversity differ from those based on phylogenetic or functional diversity. However, spatial mismatches in conservation priority regions need not indicate low surrogacy among these dimensions in conservation planning. Here, we use data for 10,213 terrestrial vertebrate species across the Americas to evaluate surrogacy; that is, the proportion of phylogenetic or functional diversity represented in conservation plans targeting species. We find that most conservation plans targeting species diversity also represent phylogenetic and functional diversity well, despite spatial mismatches in the priority regions identified by each plan. However, not all phylogenetic and functional diversity is represented within species-based plans, with the highest-surrogacy conservation strategy depending on the proportion of land area included in plans. Our results indicate that targeting species diversity could be sufficient to preserve much of the phylogenetic and functional dimensions of biodiversity in terrestrial vertebrates of the Americas. Incorporating phylogenetic and functional data in broad-scale conservation planning may not always be necessary, especially when the cost of doing so is high.

Parasponia: a novel system for studying mutualism stability.

Understanding how mutualistic interactions are stabilized in the presence of cheaters is a major question in evolutionary biology. The legume-rhizobia mutualism has become a model system for studying how plants control cheating partners. However, the generality and evolutionary origins of these control mechanisms are intensely debated. In this Opinion article, we argue that a novel system--the Parasponia-rhizobia mutualism--will significantly advance research in mutualism stability. Parasponia is the only non-legume lineage to have evolved a rhizobial symbiosis, which provides an evolutionary replicate to test how rhizobial exploitation is controlled. Evidence also suggests that this symbiosis is young. This allows studies at an earlier evolutionary stage in mutualisms, so the origin of control mechanisms can be better understood.

Slipping through the cracks: rubber plantation is unsuitable breeding habitat for frogs in Xishuangbanna, China.

Conversion of tropical forests into agriculture may present a serious risk to amphibian diversity if amphibians are not able to use agricultural areas as habitat. Recently, in Xishuangbanna Prefecture, Yunnan Province - a hotspot of frog diversity within China - two-thirds of the native tropical rainforests have been converted into rubber plantation agriculture. We conducted surveys and experiments to quantify habitat use for breeding and non-breeding life history activities of the native frog species in rainforest, rubber plantation and other human impacted sites. Rubber plantation sites had the lowest species richness in our non-breeding habitat surveys and no species used rubber plantation sites as breeding habitat. The absence of breeding was likely not due to intrinsic properties of the rubber plantation pools, as our experiments indicated that rubber plantation pools were suitable for tadpole growth and development. Rather, the absence of breeding in the rubber plantation was likely due to a misalignment of breeding and non-breeding habitat preferences. Analyses of our breeding surveys showed that percent canopy cover over pools was the strongest environmental variable influencing breeding site selection, with species exhibiting preferences for pools under both high and low canopy cover. Although rubber plantation pools had high canopy cover, the only species that bred in high canopy cover sites used the rainforest for both non-breeding and breeding activities, completing their entire life cycle in the rainforest. Conversely, the species that did use the rubber plantation for non-breeding habitat preferred to breed in low canopy sites, also avoiding breeding in the rubber plantation. Rubber plantations are likely an intermediate habitat type that 'slips through the cracks' of species habitat preferences and is thus avoided for breeding. In summary, unlike the rainforests they replaced, rubber plantations alone may not be able to support frog populations.

Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation.

There are now a number of well-studied cases in which hybridization between closely related sympatric species has increased, sometimes resulting in the replacement of species pairs by hybrid swarms. Many of these cases have been linked to anthropogenic environmental change, but the mechanisms leading from environmental change to species collapse, and the long-term effects of hybridization on species pairs, remain poorly understood. We used an individual-based stochastic simulation model to explore the conditions under which disturbances that weaken premating barriers to reproduction patterns between sympatric species might lead to increased hybridization and to species collapse. Disturbances often resulted in bouts of hybridization, but in many cases strong reproductive isolation spontaneously reemerged. This was sometimes true even after hybrid swarms had replaced parental species. The reemergence of species pairs was most likely when disturbances were of short duration. Counterintuitively, incipient species pairs were more likely to reemerge after strong but temporary disturbances than after weaker disturbances of the same duration. Even temporary bouts of hybridization often led to substantial homogenization of species pairs. This suggests that ecosystem managers may be able to refill ecological niches, but in general will not be able to resurrect lost species after species collapse.

Why does Rhinopithecus bieti prefer the highest elevation range in winter? A test of the sunshine hypothesis.

Environmental factors that affect spatiotemporal distribution patterns of animals usually include resource availability, temperature, and the risk of predation. However, they do not explain the counterintuitive preference of high elevation range in winter by the black-and-white snub-nosed monkey (Rhinopithecus bieti). We asked whether variation of sunshine along with elevations is the key driving force. To test this hypothesis, we conducted field surveys to demonstrate that there was a statistically significant pattern of high elevation use during winter. We then asked whether this pattern can be explained by certain environmental factors, namely temperature, sunshine duration and solar radiation. Finally, we concluded with a possible ecological mechanism for this pattern. In this study, we employed GIS technology to quantify solar radiation and sunshine duration across the monkey's range. Our results showed that: 1) R. bieti used the high altitude range between 4100-4400 m in winter although the yearly home range spanned from 3500-4500 m; 2) both solar radiation and sunshine duration increased with elevation while temperature decreased with elevation; 3) within the winter range, the use of range was significantly correlated with solar radiation and sunshine duration; 4) monkeys moved to the areas with high solar radiation and duration following a snowfall, where the snow melts faster and food is exposed earlier. We concluded that sunshine was the main factor that influences selection of high elevation habitat for R. bieti in winter. Since some other endotherms in the area exhibit similar winter distributional patterns, we developed a sunshine hypothesis to explain this phenomenon. In addition, our work also represented a new method of integrating GIS models into traditional field ecology research to study spatiotemporal distribution pattern of wildlife. We suggest that further theoretical and empirical studies are necessary for better understanding of sunshine influence on wildlife range use.