How cougars and feral donkeys change desert wetlands: Novel interactions between native predators and non-native megaherbivores shape trophic cascades in the Anthropocene.

Research Highlight: Lundgren, E. J., Ramp, D., Middleton, O. S., Wooster, E. I. F., Kusch, E., Balisi, M., Ripple, W. J., Hasselerharm, C. D., Sanchez, J. N., Mills, M. & Wallach, A. D. (2022) A novel trophic cascade between cougars and feral donkeys shapes desert wetlands. Journal of Animal Ecology, (91, 2010-2022). https://doi.org/10.1111/1365-2656.13766. Despite being absent from most regions of the contemporary world, megafauna species dominated the dynamics of ecological communities until the late Pleistocene. Trophic rewilding is a promising approach to restoring megafauna interactions, their functional roles and the consequent trophic cascades. Unintentional rewilding with large non-native herbivores, such as equids, offers outstanding opportunities for ecologists to understand the outcomes of using replacement species to restore the ecological functions of extinct native megafauna. In this context, it is relevant to understand the extent to which extant native predators can impose top-down control on non-native megaherbivores and how trophic cascades arising from novel predator-prey interactions influences biodiversity and ecosystem functions. In Death Valley National Park (United States), Lundgren et al. depict a natural experiment showing compelling evidence of native cougars overcoming ecological naïveté-that is, the mismatches between predator and prey species that do not share a common evolutionary history-and are now successfully preying on younger individuals of feral donkeys. These non-native donkeys, whose growing wild populations threaten the native biota, became cougars' most frequent dietary item in that region. In areas with cougars, donkeys changed their spatiotemporal foraging patterns, becoming diurnal and less active. On the other hand, donkeys remain more active and forage throughout the day and night in areas without cougars. The cougar-donkey interaction triggered a behaviourally mediated trophic cascade emerging from a 'landscape of fear', that is, from the perception of spatial heterogeneity in predation risk by donkeys. Areas with cougars have less trampled ground, fewer donkey trails, and much more canopy cover and vegetation around water. Donkeys concentrate their activity mostly in topologically plain terrains lacking proper sites for the ambush behaviour of cougars and with more intense human presence, likely acting as a shield against the predators. Lundgren et al. present a promising model system for studying the effects of fearful grazers on community structure in the context of novel ecological interactions being established in the Anthropocene. Whether the emerging cascade is transient or persistent, the relative roles of consumptive and non-consumptive effects as underlying mechanisms, and their consequences for food web structure, functioning and stability, are questions of general interest. Addressing them can help us to elucidate the costs and benefits of using non-native megaherbivores in the functional restoration of permanently invaded ecosystems.

Pesquisa em Destaque: Lundgren, E. J., Ramp, D., Middleton, O. S., Wooster, E. I. F., Kusch, E., Balisi, M., Ripple, W. J., Hasselerharm, C. D., Sanchez, J. N., Mills, M. & Wallach, A. D. (2022) A novel trophic cascade between cougars and feral donkeys shapes desert wetlands. Journal of Animal Ecology, 00:00-00. https://doi.org/10.1111/1365-2656.13766. Apesar de estarem ausentes da maioria das regiões do mundo contemporâneo, as espécies da megafauna dominaram a dinâmica das comunidades ecológicas até o Pleistoceno tardio. A refaunação trófica é uma abordagem promissora para a restauração das interações da megafauna, de seus papéis funcionais e das cascatas tróficas delas decorrentes. A refaunação não-intencional com grandes herbívoros não-nativos, tais como equídeos, oferece oportunidades extraordinárias para os ecólogos entenderem as consequências do uso de espécies substitutas para restaurar as funções ecológicas da extinta megafauna nativa. Nesse contexto, é relevante entendermos o quanto os predadores nativos atuais podem impor controle de cima para baixo sobre mega-herbívoros não-nativos, e como cascatas tróficas oriundas de novas interações predador-presa influenciam a biodiversidade e as funções ecossistêmicas. No Parque Nacional do Vale da Morte (Estados Unidos), Lundgren et al. reportam um experimento natural mostrando evidências contundentes de que onças pardas superaram a ingenuidade ecológica - i.e., os desajustes entre predadores e presas que não compartilham uma história evolutiva comum - e agora estão predando os indivíduos mais jovens de burros ferais com sucesso. Esses burros exóticos, cujas populações crescentes ameaçam a biota nativa, se tornaram o item mais frequente da dieta das onças pardas nessa região. Em áreas com onças pardas, os burros mudaram seus padrões espaço-temporais de forrageio, tornando-se diurnos e menos ativos. Por outro lado, os burros permanecem mais ativos e forrageiam durante o dia e à noite em áreas sem onças pardas. A interação entre onças pardas e burros desencadeou uma cascata trófica comportamentalmente mediada que emerge de uma "paisagem de medo", isto é, da percepção dos burros sobre a heterogeneidade espacial do risco de predação. Áreas com onças pardas tiveram menos solo pisoteado, menos trilhas de burros, e muito mais cobertura de dossel e vegetação no entorno da água. Os burros concentram a maior parte de suas atividades em terrenos topologicamente planos, os quais não apresentam lugares apropriados para o comportamento de emboscada das onças pardas e têm presença humana mais intensa, provavelmente agindo como escudos contra predadores. Lundgren et al. apresentam um sistema modelo promissor para o estudo de efeitos de pastadores temorosos sobre a estrutura comunitária no contexto de novas interações ecológicas em estabelecimento no Antropoceno. Se a cascata trófica emergente é transiente ou persistente, os papéis relativos dos efeitos diretos e indiretos como mecanismos subjacentes, e suas consequências para a estrutura, funcionamento e estabilidade da teia trófica são questões de interesse geral. Respondê-las pode nos ajudar a elucidar os custos e benefícios de usar mega-herbívoros não-nativos na restauração funcional de ecossistemas permanentemente invadidos.

Socioecological vulnerability and the risk of zoonotic disease emergence in Brazil.

In developing countries, outbreaks of zoonotic diseases (ZDs) result from intertwined ecological, socioeconomic, and demographic processes that shape conditions for (i) increased contact between vulnerable human population and wildlife in areas undergoing environmental degradation and (ii) the rapid geographic spread of infections across socially vulnerable regions. In Brazil, recent increases in environmental and social vulnerabilities, amplified by economic and political crises, are potential triggers for outbreaks. We discuss Brazilian features that favor outbreaks and show a novel quantitative method for zoonotic risk assessment. Using data on nine ZDs from 2001 to 2019, we found that the most significant causal variables were vegetation cover and city remoteness. Furthermore, 8 of 27 states presented low-level risk of ZD outbreaks. Given the ZD-bushmeat connection, we identified central hunted mammals that should be surveilled to prevent spillover events. The current challenge is to coordinate intersectoral collaboration for effective One Health management in megadiverse countries with high social vulnerability and growing environmental degradation like Brazil.

The impact of super-spreader cities, highways, and intensive care availability in the early stages of the COVID-19 epidemic in Brazil.

Although international airports served as main entry points for SARS-CoV-2, the factors driving the uneven geographic spread of COVID-19 cases and deaths in Brazil remain mostly unknown. Here we show that three major factors influenced the early macro-geographical dynamics of COVID-19 in Brazil. Mathematical modeling revealed that the "super-spreading city" of São Paulo initially accounted for more than 85% of the case spread in the entire country. By adding only 16 other spreading cities, we accounted for 98-99% of the cases reported during the first 3 months of the pandemic in Brazil. Moreover, 26 federal highways accounted for about 30% of SARS-CoV-2's case spread. As cases increased in the Brazilian interior, the distribution of COVID-19 deaths began to correlate with the allocation of the country's intensive care units (ICUs), which is heavily weighted towards state capitals. Thus, severely ill patients living in the countryside had to be transported to state capitals to access ICU beds, creating a "boomerang effect" that contributed to skew the distribution of COVID-19 deaths. Therefore, if (i) a lockdown had been imposed earlier on in spreader-capitals, (ii) mandatory road traffic restrictions had been enforced, and (iii) a more equitable geographic distribution of ICU beds existed, the impact of COVID-19 in Brazil would be significantly lower.

Interaction generalisation and demographic feedbacks drive the resilience of plant-insect networks to extinctions.

Understanding the processes driving ecological resilience, that is the extent to which systems retain their structure while absorbing perturbations, is a central challenge for theoretical and applied ecologists. Plant-insect assemblages are well-suited for the study of ecological resilience as they are species-rich and encompass a variety of ecological interactions that correspond to essential ecosystem functions. Mechanisms affecting community response to perturbations depend on both the natural history and structure of ecological interactions. Natural history attributes of the interspecific interactions, for example whether they are mutualistic or antagonistic, may affect the ecological resilience by controlling the demographic feedbacks driving ecological dynamics at the community level. Interaction generalisation may also affect resilience, by defining opportunities for interaction rewiring, the extent to which species are able to switch interactions in fluctuating environments. These natural history attributes may also interact with network structure to affect ecological resilience. Using adaptive network models, we investigated the resilience of plant-pollinator and plant-herbivore networks to species loss. We specifically investigated how fundamental natural history differences between these systems, namely the demographic consequences of the interaction and their level of generalisation-mediating rewiring opportunities-affect the resilience of dynamic ecological networks to extinctions. We also create a general benchmark for the effect of network structure on resilience simulating extinctions on theoretical networks with controlled structures. When network structure was static, pollination networks were less resilient than herbivory networks; this is related to their high levels of nestedness and the reciprocally positive feedbacks that define mutualisms, which made co-extinction cascades more likely and longer in plant-pollinator assemblages. When considering interaction rewiring, the high generalisation and the structure of pollination networks boosted their resilience to extinctions, which approached those of herbivory networks. Simulation results using theoretical networks suggested that the empirical structure of herbivory networks may protect them from collapse. Elucidating the ecological and evolutionary processes driving interaction rewiring is key to understanding the resilience of plant-insect assemblages. Accounting for rewiring requires ecologists to combine natural history with network models that incorporate feedbacks between species abundances, traits and interactions. This combination will elucidate how perturbations propagate at community level, reshaping biodiversity structure and ecosystem functions.

Compreender os processos que governam a resiliência dos sistemas ecológicos, i.e. o quanto sistemas ecológicos conservam sua estrutura enquanto absorvem perturbações, é um desafio central para ecólogos teóricos e aplicados. Comunidades de insetos e plantas são bons modelos para o estudo da resiliência ecológica pois são ricos em espécies, representando uma grande diversidade de interações ecológicas que correspondem a serviços ecossistêmicos essenciais. Os mecanismos que afetam a resposta de comunidades ecológicas a perturbações dependem tanto da história natural quanto da estrutura das interações ecológicas. A história natural de interações interespecíficas, e.g. se a interação é mutualística ou antagonística, pode afetar a resiliência do sistema ao controlar as retroalimentações demográficas que governam a dinâmica ecológica no nível da comunidade. Generalismo nas interações também pode afetar resiliência ao definir as oportunidades de rewiring de interações, i.e. o quanto espécies são capazes de mudar interações em ambientes instáveis. Atributos da história natural das interações podem também interagir com a estrutura de redes ecológicas de forma a influenciar a resiliência de sistemas ecológicos. Usando modelos de redes adaptativas, investigamos a resiliência de redes polinizador-planta e herbívoro-planta à perda de espécies. Especificamente, investigamos como diferenças fundamentais na história natural dos dois sistemas, isto é, as consequências demográficas da interação e seu grau de generalização - que mediam as oportunidades de rewiring - afetam a resiliência de redes ecológicas dinâmicas a extinções. Também criamos um referencial teórico e abrangente para o efeito da estrutura das redes em sua resiliência, simulando extinções em redes teóricas com estruturas controladas. Quando a estrutura das redes foi considerada estática, redes de polinização foram menos resilientes do que redes de herbivoria; o que está associado aos maiores níveis de aninhamento e aos efeitos demográficos positivos e recíprocos que definem mutualismos, aumentando a probabilidade e o comprimento das cascatas de extinção em redes polinizador-planta. Ao incorporar rewiring de interações, a alta generalização e a estrutura das redes de polinização impulsionou sua resiliência a extinções, que se aproximou da resiliência de redes de herbivoria. Os resultados das simulações com redes teóricas sugerem que estrutura de redes de herbivoria protegem esses sistemas do colapso. Compreender quais processos ecológicos e evolutivos governam o rewiring de interações é chave se queremos prever a resiliência de sistemas inseto-planta. Para incorporar rewiring de interações, será necessário combinar conhecimento sobre história natural com modelos de rede que incorporem a retroalimentação entre abundâncias, atributos e interações das espécies envolvidas. Essa combinação elucidará como perturbações se propagam no nível de comunidades ecológicas, reconfigurando a estrutura da biodiversidade e suas funções ecossistêmicas.

Vulnerability of the micro-regions of the South of Brazil to the new coronavirus (SARS-CoV-2) pandemic / Vulnerabilidade das microrregiões da Região Sul do Brasil à pandemia do novo coronavírus (SARS-CoV-2)

This is the first report of the 'Observatório COVID191 - Grupo: Redes de Contágio ­ Laboratório de Estudos de Defesa' for the South region of Brazil. We have combined data of confirmed cases of the new coronavirus (SARS-CoV-2) for the South available up to 17/04/2020, with structural analyses of road networks, from within and between states, to estimate the vulnerability and potential influence of the South micro-regions to propagate the disease.

Este é o primeiro relatório do Observatório COVID19 - Grupo: Redes de Contágio ­ Laboratório de Estudos de Defesa para a região Sul do Brasil. Combinamos dados de casos confirmados do novo coronavírus (SARS-CoV-2) para o Sul, disponíveis até o dia 17/04/2020, com análises estruturais da rede de rotas rodoviárias intra e interestaduais para estimarmos a vulnerabilidade e potencial influência das microrregiões sulinas na propagação da doença.

Adaptive Networks for Restoration Ecology.

The urgent need to restore biodiversity and ecosystem functioning challenges ecology as a predictive science. Restoration ecology would benefit from evolutionary principles embedded within a framework that combines adaptive network models and the phylogenetic structure of ecological interactions. Adaptive network models capture feedbacks between trait evolution, species abundances, and interactions to explain resilience and functional diversity within communities. Phylogenetically-structured network data, increasingly available via next-generation sequencing, inform constraints affecting interaction rewiring. Combined, these approaches can predict eco-evolutionary changes triggered by community manipulation practices, such as translocations and eradications of invasive species. We discuss theoretical and methodological opportunities to bridge network models and data from restoration projects and propose how this can be applied to the functional restoration of ecological interactions.

Does biological intimacy shape ecological network structure? A test using a brood pollination mutualism on continental and oceanic islands.

Biological intimacy-the degree of physical proximity or integration of partner taxa during their life cycles-is thought to promote the evolution of reciprocal specialization and modularity in the networks formed by co-occurring mutualistic species, but this hypothesis has rarely been tested. Here, we test this "biological intimacy hypothesis" by comparing the network architecture of brood pollination mutualisms, in which specialized insects are simultaneously parasites (as larvae) and pollinators (as adults) of their host plants to that of other mutualisms which vary in their biological intimacy (including ant-myrmecophyte, ant-extrafloral nectary, plant-pollinator and plant-seed disperser assemblages). We use a novel dataset sampled from leafflower trees (Phyllanthaceae: Phyllanthus s. l. [Glochidion]) and their pollinating leafflower moths (Lepidoptera: Epicephala) on three oceanic islands (French Polynesia) and compare it to equivalent published data from congeners on continental islands (Japan). We infer taxonomic diversity of leafflower moths using multilocus molecular phylogenetic analysis and examine several network structural properties: modularity (compartmentalization), reciprocality (symmetry) of specialization and algebraic connectivity. We find that most leafflower-moth networks are reciprocally specialized and modular, as hypothesized. However, we also find that two oceanic island networks differ in their modularity and reciprocal specialization from the others, as a result of a supergeneralist moth taxon which interacts with nine of 10 available hosts. Our results generally support the biological intimacy hypothesis, finding that leafflower-moth networks (usually) share a reciprocally specialized and modular structure with other intimate mutualisms such as ant-myrmecophyte symbioses, but unlike nonintimate mutualisms such as seed dispersal and nonintimate pollination. Additionally, we show that generalists-common in nonintimate mutualisms-can also evolve in intimate mutualisms, and that their effect is similar in both types of assemblages: once generalists emerge they reshape the network organization by connecting otherwise isolated modules.

Nestedness across biological scales.

Biological networks pervade nature. They describe systems throughout all levels of biological organization, from molecules regulating metabolism to species interactions that shape ecosystem dynamics. The network thinking revealed recurrent organizational patterns in complex biological systems, such as the formation of semi-independent groups of connected elements (modularity) and non-random distributions of interactions among elements. Other structural patterns, such as nestedness, have been primarily assessed in ecological networks formed by two non-overlapping sets of elements; information on its occurrence on other levels of organization is lacking. Nestedness occurs when interactions of less connected elements form proper subsets of the interactions of more connected elements. Only recently these properties began to be appreciated in one-mode networks (where all elements can interact) which describe a much wider variety of biological phenomena. Here, we compute nestedness in a diverse collection of one-mode networked systems from six different levels of biological organization depicting gene and protein interactions, complex phenotypes, animal societies, metapopulations, food webs and vertebrate metacommunities. Our findings suggest that nestedness emerge independently of interaction type or biological scale and reveal that disparate systems can share nested organization features characterized by inclusive subsets of interacting elements with decreasing connectedness. We primarily explore the implications of a nested structure for each of these studied systems, then theorize on how nested networks are assembled. We hypothesize that nestedness emerges across scales due to processes that, although system-dependent, may share a general compromise between two features: specificity (the number of interactions the elements of the system can have) and affinity (how these elements can be connected to each other). Our findings suggesting occurrence of nestedness throughout biological scales can stimulate the debate on how pervasive nestedness may be in nature, while the theoretical emergent principles can aid further research on commonalities of biological networks.

Conflicting selection in the course of adaptive diversification: the interplay between mutualism and intraspecific competition.

Adaptive speciation can occur when a population undergoes assortative mating and disruptive selection caused by frequency-dependent intraspecific competition. However, other interactions, such as mutualisms based on trait matching, may generate conflicting selective pressures that constrain species diversification. We used individual-based simulations to explore how different types of mutualism affect adaptive diversification. A magic trait was assumed to simultaneously mediate mate choice, intraspecific competition, and mutualisms. In scenarios of intimate, specialized mutualisms, individuals interact with one or few individual mutualistic partners, and diversification is constrained only if the mutualism is obligate. In other scenarios, increasing numbers of different partners per individual limit diversification by generating stabilizing selection. Stabilizing selection emerges from the greater likelihood of trait mismatches for rare, extreme phenotypes than for common intermediate phenotypes. Constraints on diversification imposed by increased numbers of partners decrease if the trait matching degree has smaller positive effects on fitness. These results hold after the relaxation of various assumptions. When trait matching matters, mutualism-generated stabilizing selection would thus often constrain diversification in obligate mutualisms, such as ant-myrmecophyte associations, and in low-intimacy mutualisms, including plant-seed disperser systems. Hence, different processes, such as trait convergence favoring the incorporation of nonrelated species, are needed to explain the higher richness of low-intimacy assemblages--shown here to be up to 1 order of magnitude richer than high-intimacy systems.

Assemblages of endophagous insects on Asteraceae in São Paulo cerrados.

A survey of the endophagous insects fauna associated to Asteraceae capitula was carried out from 2000 to 2002 in eight cerrado sensu stricto sites located in the Brazilian state of Sdo Paulo. Sixty-four endophagous species of Diptera and Lepidoptera were recorded from 49 asteracean host plants. Approximately half of the species were obtained from a single locality, with a large proportion emerging from a single sample (unicates). Thirty percent of the species were singletons (i.e. only one individual was recorded). The large proportion of rare species suggests a high species turnover among localities. Lepidopteran species were recorded on more host species than dipterans, confirming their more polyphagous food habit, also observed in other Brazilian biomes and in Europe. We conclude that the studied cerrado localities, all within São Paulo State, are isolated with its invertebrate fauna composed of many rare and exclusive species. We suggest that the maintenance of Asteraceae biodiversity and their endophagous insects depend on the conservation of all cerrado remnants in the state.

Assemblages of endophagous insects on Asteraceae in São Paulo Cerrados

A survey of the endophagous insects fauna associated to Asteraceae capitula was carried out from 2000 to 2002 in eight cerrado sensu stricto sites located in the Brazilian state of São Paulo. Sixty-four endophagous species of Diptera and Lepidoptera were recorded from 49 asteracean host plants. Approximately half of the species were obtained from a single locality, with a large proportion emerging from a single sample (unicates). Thirty percent of the species were singletons (i.e. only one individual was recorded). The large proportion of rare species suggests a high species turnover among localities. Lepidopteran species were recorded on more host species than dipterans, confirming their more polyphagous food habit, also observed in other Brazilian biomes and in Europe. We conclude that the studied cerrado localities, all within São Paulo State, are isolated with its invertebrate fauna composed of many rare and exclusive species. We suggest that the maintenance of Asteraceae biodiversity and their endophagous insects depend on the conservation of all cerrado remnants in the state.

No presente estudo foi realizado um levantamento da fauna de insetos endófagos de capítulos de Asteraceae (Compostas), de 2000 a 2002, em oito localidades de cerrados sensu stricto no estado de São Paulo. Foram obtidas 64 espécies de endófagos (dípteros e lepidópteros) de 49 espécies de hospedeiras. Aproximadamente metade das espécies foi obtida de apenas uma área, e destas uma grande proporção ocorreu em apenas uma amostra (unicatas). Trinta por cento das espécies foram consideradas "singletons" (apenas um indivíduo foi obtido). A grande quantidade de espécies raras sugere uma forte troca de espécies entre diferentes áreas. Lepidópteros foram registrados em mais espécies hospedeiras que dípteros, confirmando o já observado para o mesmo sistema de insetos e plantas em outros ambientes no Brasil e Europa. As áreas de cerrado sensu stricto estudadas no estado de São Paulo encontram-se isoladas, com uma grande parte da fauna de invertebrados composta por muitas espécies raras e exclusivas. Diante deste quadro, sugere-se que a manutenção da biodiversidade de Asteraceae e seus endófagos em seus níveis atuais depende da conservação de todo o conjunto de remanescentes de cerrado do estado.