Ranavirus and helminth parasite co-infection in invasive American bullfrogs in the Atlantic forest, Brazil.

Emerging infectious diseases threaten amphibian species across the globe. In Brazil, the American bullfrog (Aquarana catesbeiana) is a highly invasive species that can potentially transmit parasites and pathogens to native amphibians. This is the first assessment of co-infection of Ranavirus and helminth macroparasites in invasive populations of bullfrogs in South America. We collected, measured, and euthanized 65 specimens of A. catesbeiana sampled from 9 sites across three states of Brazil in the Atlantic Forest biome. We collected and identified helminth macroparasites and sampled host liver tissue to test for the presence and load of Ranavirus with quantitative PCR. We documented patterns of prevalence, parasite load, and co-infection with generalized linear mixed models, generalized logistic regressions, and randomization tests. Most individual bullfrogs did not exhibit clinical signs of infection, but the overall Ranavirus prevalence was 27% (95% confidence interval, [CI 17-38]). Bullfrogs were infected with helminth macroparasites from 5 taxa. Co-infection of helminth macroparasites and Ranavirus was also common (21% CI [12-31]). Bullfrog size was positively correlated with total macroparasite abundance and richness, and the best-fitting model included a significant interaction between bullfrog size and Ranavirus infection status. We observed a negative correlation between Ranavirus viral load and nematode abundance (slope = -0.22, P = 0.03). Invasive bullfrogs (A. catesbeiana) in Brazil were frequently infected with both Ranavirus and helminth macroparasites, so adult bullfrogs could serve as reservoir hosts for both pathogens and parasites. However, many macroparasites collected were encysted and not developing. Coinfection patterns suggest a potential interaction between Ranavirus and macroparasites because helminth abundance increased with bullfrog size but was lower in Ranavirus infected individuals. Future studies of bullfrogs in the Atlantic Forest should investigate their potential role in pathogen and parasite transmission to native anurans.

High prevalence and concomitant infection of Ranavirus and Eustrongylides sp. in the invasive American Bullfrog in Brazil.

American Bullfrogs, Aquarana catesbeiana, are invasive anuran species distributed worldwide. One of the adverse impacts that this species causes in native communities is as a reservoir host for pathogens and parasites. Here, we report the coinfection of two pathogenic organisms in A. catesbeiana: Ranavirus and the nematode Eustrongylides. Bullfrogs were collected in the wild in a pond close to the urban area of São Paulo, Brazil. The prevalence of both pathogens was high: 77% were infected with ranavirus with a mean viral load of 1010.3 viral copies, and 100% of the bullfrogs were infected by Eustrongylides sp. with a mean intensity of infection of 13.4 specimens per host. Four host specimens (31%) presented pathological signs that seemed to be related to the Eustrongylides sp. infection, such as internal organs adhered to each other due to high intensity and large size of the nematodes, ulcers, and raw flesh wounds caused by the nematode. The pathogenic and concomitant infections have potential zoonotic implications and raise concerns about human infection risks for Eustrongylides infection. Moreover, such infections may represent an additional level of threat to native communities through the potential shifts in patterns of parasite and pathogen transmission. Future research involving the native anuran community is essential to ascertain whether invasive bullfrogs are attenuating or exacerbating diseases such as ranavirosis and eustrongylidiosis.

Synthesis reveals approximately balanced biotic differentiation and homogenization.

It is commonly thought that the biodiversity crisis includes widespread declines in the spatial variation of species composition, called biotic homogenization. Using a typology relating homogenization and differentiation to local and regional diversity changes, we synthesize patterns across 461 metacommunities surveyed for 10 to 91 years, and 64 species checklists (13 to 500+ years). Across all datasets, we found that no change was the most common outcome, but with many instances of homogenization and differentiation. A weak homogenizing trend of a 0.3% increase in species shared among communities/year on average was driven by increased numbers of widespread (high occupancy) species and strongly associated with checklist data that have longer durations and large spatial scales. At smaller spatial and temporal scales, we show that homogenization and differentiation can be driven by changes in the number and spatial distributions of both rare and common species. The multiscale perspective introduced here can help identify scale-dependent drivers underpinning biotic differentiation and homogenization.

Operationalizing cultural adaptation to climate change: contemporary examples from United States agriculture.

It has been proposed that climate adaptation research can benefit from an evolutionary approach. But related empirical research is lacking. We advance the evolutionary study of climate adaptation with two case studies from contemporary United States agriculture. First, we define 'cultural adaptation to climate change' as a mechanistic process of population-level cultural change. We argue this definition enables rigorous comparisons, yields testable hypotheses from mathematical theory and distinguishes adaptive change, non-adaptive change and desirable policy outcomes. Next, we develop an operational approach to identify 'cultural adaptation to climate change' based on established empirical criteria. We apply this approach to data on crop choices and the use of cover crops between 2008 and 2021 from the United States. We find evidence that crop choices are adapting to local trends in two separate climate variables in some regions of the USA. But evidence suggests that cover cropping may be adapting more to the economic environment than climatic conditions. Further research is needed to characterize the process of cultural adaptation, particularly the routes and mechanisms of cultural transmission. Furthermore, climate adaptation policy could benefit from research on factors that differentiate regions exhibiting adaptive trends in crop choice from those that do not. This article is part of the theme issue 'Climate change adaptation needs a science of culture'.

Time-travelling pathogens and their risk to ecological communities.

Permafrost thawing and the potential 'lab leak' of ancient microorganisms generate risks of biological invasions for today's ecological communities, including threats to human health via exposure to emergent pathogens. Whether and how such 'time-travelling' invaders could establish in modern communities is unclear, and existing data are too scarce to test hypotheses. To quantify the risks of time-travelling invasions, we isolated digital virus-like pathogens from the past records of coevolved artificial life communities and studied their simulated invasion into future states of the community. We then investigated how invasions affected diversity of the free-living bacteria-like organisms (i.e., hosts) in recipient communities compared to controls where no invasion occurred (and control invasions of contemporary pathogens). Invading pathogens could often survive and continue evolving, and in a few cases (3.1%) became exceptionally dominant in the invaded community. Even so, invaders often had negligible effects on the invaded community composition; however, in a few, highly unpredictable cases (1.1%), invaders precipitated either substantial losses (up to -32%) or gains (up to +12%) in the total richness of free-living species compared to controls. Given the sheer abundance of ancient microorganisms regularly released into modern communities, such a low probability of outbreak events still presents substantial risks. Our findings therefore suggest that unpredictable threats so far confined to science fiction and conjecture could in fact be powerful drivers of ecological change.

Looking back on biodiversity change: lessons for the road ahead.

Estimating biodiversity change across the planet in the context of widespread human modification is a critical challenge. Here, we review how biodiversity has changed in recent decades across scales and taxonomic groups, focusing on four diversity metrics: species richness, temporal turnover, spatial beta-diversity and abundance. At local scales, change across all metrics includes many examples of both increases and declines and tends to be centred around zero, but with higher prevalence of declining trends in beta-diversity (increasing similarity in composition across space or biotic homogenization) and abundance. The exception to this pattern is temporal turnover, with changes in species composition through time observed in most local assemblages. Less is known about change at regional scales, although several studies suggest that increases in richness are more prevalent than declines. Change at the global scale is the hardest to estimate accurately, but most studies suggest extinction rates are probably outpacing speciation rates, although both are elevated. Recognizing this variability is essential to accurately portray how biodiversity change is unfolding, and highlights how much remains unknown about the magnitude and direction of multiple biodiversity metrics at different scales. Reducing these blind spots is essential to allow appropriate management actions to be deployed. This article is part of the theme issue 'Detecting and attributing the causes of biodiversity change: needs, gaps and solutions'.

Six decades of museum collections reveal disruption of native ant assemblages by introduced species.

There is a looming environmental crisis characterized by widespread declines in global biodiversity,1,2,3,4,5,6 coupled with the establishment of introduced species at accelerated rates.7,8,9,10,11,12,13,14 We quantified how multi-species invasions affect litter ant communities in natural ecosystems by leveraging museum records and contemporary collections to assemble a large (18,990 occurrences, 6,483 sampled local communities, and 177 species) 54-year (1965-2019) dataset for the entire state of Florida, USA. Nine of ten species that decreased most strongly in relative abundance ("losers") were native, while nine of the top ten "winners" were introduced species. These changes led to shifts in the composition of rare and common species: in 1965, only two of the ten most common ants were introduced, whereas by 2019, six of ten were introduced species. Native losers included seed dispersers and specialist predators, suggesting a potential loss of ecosystem function through time, despite no obvious loss of phylogenetic diversity. We also examined the role of species-level traits as predictors of invasion success. Introduced species were more likely to be polygynous than native species. The tendency to form supercolonies, where workers from separate nests integrate, also differed between native and introduced species and was correlated with the degree to which species increased in their rank abundances over 50 years. In Florida, introduced ants now account for 30% of occurrence records, and up to 70% in southern Florida. If current trends continue, introduced species will account for over half of occurrence records in all Florida's litter ant communities within the next 50 years.

Regional occupancy increases for widespread species but decreases for narrowly distributed species in metacommunity time series.

While human activities are known to elicit rapid turnover in species composition through time, the properties of the species that increase or decrease their spatial occupancy underlying this turnover are less clear. Here, we used an extensive dataset of 238 metacommunity time series of multiple taxa spread across the globe to evaluate whether species that are more widespread (large-ranged species) differed in how they changed their site occupancy over the 10-90 years the metacommunities were monitored relative to species that are more narrowly distributed (small-ranged species). We found that on average, large-ranged species tended to increase in occupancy through time, whereas small-ranged species tended to decrease. These relationships were stronger in marine than in terrestrial and freshwater realms. However, in terrestrial regions, the directional changes in occupancy were less extreme in protected areas. Our findings provide evidence for systematic decreases in occupancy of small-ranged species, and that habitat protection could mitigate these losses in the face of environmental change.

How does variation in total and relative abundance contribute to gradients of species diversity?

Patterns of biodiversity provide insights into the processes that shape biological communities around the world. Variation in species diversity along biogeographical or ecological gradients, such as latitude or precipitation, can be attributed to variation in different components of biodiversity: changes in the total abundance (i.e., more-individual effects) and changes in the regional species abundance distribution (SAD). Rarefaction curves can provide a tool to partition these sources of variation on diversity, but first must be converted to a common unit of measurement. Here, we partition species diversity gradients into components of the SAD and abundance using the effective number of species (ENS) transformation of the individual-based rarefaction curve. Because the ENS curve is unconstrained by sample size, it can act as a standardized unit of measurement when comparing effect sizes among different components of biodiversity change. We illustrate the utility of the approach using two data sets spanning latitudinal diversity gradients in trees and marine reef fish and find contrasting results. Whereas the diversity gradient of fish was mostly associated with variation in abundance (86%), the tree diversity gradient was mostly associated with variation in the SAD (59%). These results suggest that local fish diversity may be limited by energy through the more-individuals effect, while species pool effects are the larger determinant of tree diversity. We suggest that the framework of the ENS-curve has the potential to quantify the underlying factors influencing most aspects of diversity change.

Late quaternary biotic homogenization of North American mammalian faunas.

Biotic homogenization-increasing similarity of species composition among ecological communities-has been linked to anthropogenic processes operating over the last century. Fossil evidence, however, suggests that humans have had impacts on ecosystems for millennia. We quantify biotic homogenization of North American mammalian assemblages during the late Pleistocene through Holocene (~30,000 ybp to recent), a timespan encompassing increased evidence of humans on the landscape (~20,000-14,000 ybp). From ~10,000 ybp to recent, assemblages became significantly more homogenous (>100% increase in Jaccard similarity), a pattern that cannot be explained by changes in fossil record sampling. Homogenization was most pronounced among mammals larger than 1 kg and occurred in two phases. The first followed the megafaunal extinction at ~10,000 ybp. The second, more rapid phase began during human population growth and early agricultural intensification (~2,000-1,000 ybp). We show that North American ecosystems were homogenizing for millennia, extending human impacts back ~10,000 years.

Local biodiversity change reflects interactions among changing abundance, evenness, and richness.

Biodiversity metrics often integrate data on the presence and abundance of multiple species. Yet our understanding of covariation between changes to the numbers of individuals, the evenness of species relative abundances, and the total number of species remains limited. Using individual-based rarefaction curves, we show how expected positive relationships among changes in abundance, evenness and richness arise, and how they can break down. We then examined interdependencies between changes in abundance, evenness and richness in more than 1100 assemblages sampled either through time or across space. As predicted, richness changes were greatest when abundance and evenness changed in the same direction, and countervailing changes in abundance and evenness acted to constrain the magnitude of changes in species richness. Site-to-site differences in abundance, evenness, and richness were often decoupled, and pairwise relationships between these components across assemblages were weak. In contrast, changes in species richness and relative abundance were strongly correlated for assemblages varying through time. Temporal changes in local biodiversity showed greater inertia and stronger relationships between the component changes when compared to site-to-site variation. Overall, local variation in assemblage diversity was rarely due to repeated passive samples from an approximately static species abundance distribution. Instead, changing species relative abundances often dominated local variation in diversity. Moreover, how changing relative abundances combined with changes to total abundance frequently determined the magnitude of richness changes. Embracing the interdependencies between changing abundance, evenness and richness can provide new information to better understand biodiversity change in the Anthropocene.

Source-sink behavioural dynamics limit institutional evolution in a group-structured society.

Social change in any society entails changes in both behaviours and institutions. We model a group-structured society in which the transmission of individual behaviour occurs in parallel with the selection of group-level institutions. We consider a cooperative behaviour that generates collective benefits for groups but does not spread between individuals on its own. Groups exhibit institutions that increase the diffusion of the behaviour within the group, but also incur a group cost. Groups adopt institutions in proportion to their fitness. Finally, the behaviour may also spread globally. We find that behaviour and institutions can be mutually reinforcing. But the model also generates behavioural source-sink dynamics when behaviour generated in institutionalized groups spreads to non-institutionalized groups and boosts their fitness. Consequently, the global diffusion of group-beneficial behaviour creates a pattern of institutional free-riding that limits the evolution of group-beneficial institutions. Our model suggests that, in a group-structured society, large-scale beneficial social change can be best achieved when the relevant behaviour and institutions remain correlated.

Random placement models explain species richness and dissimilarity of frog assemblages within Atlantic Forest fragments.

Understanding the effects of random versus niche-based processes on biodiversity patterns is a central theme in ecology, and an important tool for predicting effects of habitat loss and fragmentation on biodiversity. We investigated the predictive power of random processes to explain species richness and species dissimilarity of amphibian assemblages in a fragmented tropical landscape of the Atlantic Forest of South America. We analyzed a large database of amphibian abundance and occupancy, sampled in 21 forest fragments ranging in size from 1.9 to 619 ha. We compared observed species richness and species dissimilarity with the outcomes of two null (random placement) models: 1- the traditional Coleman's area-based model and 2- an abundance-based model (based on the number of individuals observed in each fragment). We applied these models for all species combined, and separately for forest-dependent and habitat-generalist species. The abundance-based model fitted the observed species richness data better than the area-based model for all species, forest-dependent species, and generalist species. The area-based and the abundance-based models were also able to significantly explain species dissimilarity for all species and for generalists, but not for forest dependent species. The traditional area-based model assigned too many individuals to large fragments, thus failing to accurately explain species richness within patches across the landscape. Although niche-based processes may be important to structuring the regional pool of species in fragmented landscapes, our results suggest that part of the variation in species richness and species dissimilarity can be successfully explained by random placement models, especially for generalist species. Evaluating which factors cause variation in the number of individuals among patches should be a focus in future studies aiming to understand biodiversity patterns in fragmented landscapes.

Compreender os efeitos de processos aleatórios versus processos baseados em nicho nos padrões de biodiversidade é um tema central em ecologia e uma ferramenta importante para prever os efeitos da perda e fragmentação de habitat na biodiversidade. Nós investigamos o poder preditivo de processos aleatórios para explicar a riqueza e a dissimilaridade de espécies de assembleias de anfíbios em uma paisagem fragmentada tropical da Mata Atlântica da América do Sul. Analisamos um grande conjunto de dados de abundância e ocupação de anfíbios, amostrados em 21 fragmentos florestais com tamanhos de 1.9 a 619 ha. Comparamos a riqueza e a dissimilaridade de espécies observadas com os resultados de dois modelos nulos (posicionamento aleatório): 1- o modelo tradicional baseado em área de Coleman e 2 - um modelo baseado em abundância (com base no número de indivíduos observados em cada fragmento). Aplicamos esses modelos para todas as espécies combinadas e separadamente para espécies dependentes de floresta e espécies generalistas de habitat. O modelo baseado em abundância ajustou-se melhor aos dados observados de riqueza de espécies do que o modelo baseado em área para todas as espécies, espécies dependentes de floresta e espécies generalistas. Os modelos baseados em área e em abundância também foram capazes de explicar significativamente a dissimilaridade de espécies para todas as espécies e para generalistas, mas não para espécies dependentes de floresta. O modelo tradicional baseado em área atribuiu muitos indivíduos a grandes fragmentos, falhando assim em explicar com precisão a riqueza de espécies dentro de manchas na paisagem. Embora processos baseados em nicho possam ser importantes para estruturar o conjunto regional de espécies em paisagens fragmentadas, nossos resultados sugerem que parte da variação na riqueza e dissimilaridade de espécies pode ser explicada com sucesso por modelos de posicionamento aleatório, especialmente para espécies generalistas. Avaliar quais fatores causam variação no número de indivíduos entre manchas deve ser um foco em estudos futuros que visem compreender os padrões de biodiversidade em paisagens fragmentadas.

Long-term changes in temperate marine fish assemblages are driven by a small subset of species.

The species composition of plant and animal assemblages across the globe has changed substantially over the past century. How do the dynamics of individual species cause this change? We classified species into seven unique categories of temporal dynamics based on the ordered sequence of presences and absences that each species contributes to an assemblage time series. We applied this framework to 14,434 species trajectories comprising 280 assemblages of temperate marine fishes surveyed annually for 20 or more years. Although 90% of the assemblages diverged in species composition from the baseline year, this compositional change was largely driven by only 8% of the species' trajectories. Quantifying the reorganization of assemblages based on species shared temporal dynamics should facilitate the task of monitoring and restoring biodiversity. We suggest ways in which our framework could provide informative measures of compositional change, as well as leverage future research on pattern and process in ecological systems.

Environment-host-microbial interactions shape the Sarracenia purpurea microbiome at the continental scale.

The importance of climate, habitat structure, and higher trophic levels on microbial diversity is only beginning to be understood. Here, we examined the influence of climate variables, plant morphology, and the abundance of aquatic invertebrates on the microbial biodiversity of the northern pitcher plant Sarracenia purpurea. The plant's cup-shaped leaves fill with rainwater and support a miniature, yet full-fledged, ecosystem with a diverse microbiome that decomposes captured prey and a small network of shredding and filter-feeding aquatic invertebrates that feed on microbes. We characterized pitcher microbiomes of 108 plants sampled at 36 sites from Florida to Quebec. Structural equation models revealed that annual precipitation and temperature, plant size, and midge abundance had direct effects on microbiome taxonomic and phylogenetic diversity. Climate variables also exerted indirect effects through plant size and midge abundance. Further, spatial structure and climate influenced taxonomic composition, but not phylogenetic composition. Our results suggest that direct effects of midge abundance and climate and indirect effects of climate through its effect on plant-associated factors lead to greater richness of microbial phylotypes in warmer, wetter sites.

Investigating Biotic Interactions in Deep Time.

Recent renewed interest in using fossil data to understand how biotic interactions have shaped the evolution of life is challenging the widely held assumption that long-term climate changes are the primary drivers of biodiversity change. New approaches go beyond traditional richness and co-occurrence studies to explicitly model biotic interactions using data on fossil and modern biodiversity. Important developments in three primary areas of research include analysis of (i) macroevolutionary rates, (ii) the impacts of and recovery from extinction events, and (iii) how humans (Homo sapiens) affected interactions among non-human species. We present multiple lines of evidence for an important and measurable role of biotic interactions in shaping the evolution of communities and lineages on long timescales.

Using Climatic Credits to Pay the Climatic Debt.

Many organisms are accumulating climatic debt as they respond more slowly than expected to rising global temperatures, leading to disequilibrium of species diversity with contemporary climate. The resulting transient dynamics are complex and may cause overoptimistic biodiversity assessments. We propose a simple budget framework to integrate climatic debt with two classes of intervention: (i) climatic credits that pay some of the debt, reducing the overall biological change required to reach a new equilibrium; and (ii) options to adjust the debt repayment rate, either making a system more responsive by increasing the rate or temporarily reducing the rate to buy more time for local adaptation and credit implementation. We illustrate how this budget can be created and highlight limitations and challenges.

A multiscale framework for disentangling the roles of evenness, density, and aggregation on diversity gradients.

Disentangling the drivers of diversity gradients can be challenging. The Measurement of Biodiversity (MoB) framework decomposes scale-dependent changes in species diversity into three components of community structure: species abundance distribution (SAD), total community abundance, and within-species spatial aggregation. Here we extend MoB from categorical treatment comparisons to quantify variation along continuous geographic or environmental gradients. Our approach requires sites along a gradient, each consisting of georeferenced plots of abundance-based species composition data. We demonstrate our method using a case study of ants sampled along an elevational gradient of 28 sites in a mixed deciduous forest of the Great Smoky Mountains National Park, USA. MoB analysis revealed that decreases in ant species richness along the elevational gradient were associated with decreasing evenness and total number of species, which counteracted the modest increase in richness associated with decreasing spatial aggregation along the gradient. Total community abundance had a negligible effect on richness at all but the finest spatial grains, SAD effects increased in importance with sampling effort, and the aggregation effect had the strongest effect at coarser spatial grains. These results do not support the more-individuals hypothesis, but they are consistent with a hypothesis of stronger environmental filtering at coarser spatial grains. Our extension of MoB has the potential to elucidate how components of community structure contribute to changes in diversity along environmental gradients and should be useful for a variety of assemblage-level data collected along gradients.

Clockwise and counterclockwise hysteresis characterize state changes in the same aquatic ecosystem.

Incremental increases in a driver variable, such as nutrients or detritus, can trigger abrupt shifts in aquatic ecosystems that may exhibit hysteretic dynamics and a slow return to the initial state. A model system for understanding these dynamics is the microbial assemblage that inhabits the cup-shaped leaves of the pitcher plant Sarracenia purpurea. With enrichment of organic matter, this system flips within three days from an oxygen-rich state to an oxygen-poor state. In a replicated greenhouse experiment, we enriched pitcher-plant leaves at different rates with bovine serum albumin (BSA), a molecular substitute for detritus. Changes in dissolved oxygen (DO) and undigested BSA concentration were monitored during enrichment and recovery phases. With increasing enrichment rates, the dynamics ranged from clockwise hysteresis (low), to environmental tracking (medium), to novel counter-clockwise hysteresis (high). These experiments demonstrate that detrital enrichment rate can modulate a diversity of hysteretic responses within a single aquatic ecosystem, and suggest different management strategies may be needed to mitigate the effects of high vs. low rates of detrital enrichment.

Trade-Offs in Cold Resistance at the Northern Range Edge of the Common Woodland Ant Aphaenogaster picea (Formicidae).

Geographic variation in low temperatures at poleward range margins of terrestrial species often mirrors population variation in cold resistance, suggesting that range boundaries may be set by evolutionary constraints on cold physiology. The northeastern woodland ant Aphaenogaster picea occurs up to approximately 45°N in central Maine. We combined presence/absence surveys with classification tree analysis to characterize its northern range limit and assayed two measures of cold resistance operating on different timescales to determine whether and how marginal populations adapt to environmental extremes. The range boundary of A. picea was predicted primarily by temperature, but low winter temperatures did not emerge as the primary correlate of species occurrence. Low summer temperatures and high seasonal variability predicted absence above the boundary, whereas high mean annual temperature (MAT) predicted presence in southern Maine. In contrast, assays of cold resistance across multiple sites were consistent with the hypothesis of local cold adaptation at the range edge: among populations, there was a 4-min reduction in chill coma recovery time across a 2° reduction in MAT. Baseline resistance and capacity for additional plastic cold hardening shifted in opposite directions, with hardening capacity approaching zero at the coldest sites. This trade-off between baseline resistance and cold-hardening capacity suggests that populations at range edges may adapt to colder temperatures through genetic assimilation of plastic responses, potentially constraining further adaptation and range expansion.