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.

Congruent trophic pathways underpin global coral reef food webs.

Ecological interactions uphold ecosystem structure and functioning. However, as species richness increases, the number of possible interactions rises exponentially. More than 6,000 species of coral reef fishes exist across the world's tropical oceans, resulting in an almost innumerable array of possible trophic interactions. Distilling general patterns in these interactions across different bioregions stands to improve our understanding of the processes that govern coral reef functioning. Here, we show that across bioregions, tropical coral reef food webs exhibit a remarkable congruence in their trophic interactions. Specifically, by compiling and investigating the structure of six coral reef food webs across distinct bioregions, we show that when accounting for consumer size and resource availability, these food webs share more trophic interactions than expected by chance. In addition, coral reef food webs are dominated by dietary specialists, which makes trophic pathways vulnerable to biodiversity loss. Prey partitioning among these specialists is geographically consistent, and this pattern intensifies when weak interactions are disregarded. Our results suggest that energy flows through coral reef communities along broadly comparable trophic pathways. Yet, these critical pathways are maintained by species with narrow, specialized diets, which threatens the existence of coral reef functioning in the face of biodiversity loss.

Estimating co-extinction threats in terrestrial ecosystems.

The biosphere is changing rapidly due to human endeavour. Because ecological communities underlie networks of interacting species, changes that directly affect some species can have indirect effects on others. Accurate tools to predict these direct and indirect effects are therefore required to guide conservation strategies. However, most extinction-risk studies only consider the direct effects of global change-such as predicting which species will breach their thermal limits under different warming scenarios-with predictions of trophic cascades and co-extinction risks remaining mostly speculative. To predict the potential indirect effects of primary extinctions, data describing community interactions and network modelling can estimate how extinctions cascade through communities. While theoretical studies have demonstrated the usefulness of models in predicting how communities react to threats like climate change, few have applied such methods to real-world communities. This gap partly reflects challenges in constructing trophic network models of real-world food webs, highlighting the need to develop approaches for quantifying co-extinction risk more accurately. We propose a framework for constructing ecological network models representing real-world food webs in terrestrial ecosystems and subjecting these models to co-extinction scenarios triggered by probable future environmental perturbations. Adopting our framework will improve estimates of how environmental perturbations affect whole ecological communities. Identifying species at risk of co-extinction (or those that might trigger co-extinctions) will also guide conservation interventions aiming to reduce the probability of co-extinction cascades and additional species losses.

Delineating reef fish trophic guilds with global gut content data synthesis and phylogeny.

Understanding species' roles in food webs requires an accurate assessment of their trophic niche. However, it is challenging to delineate potential trophic interactions across an ecosystem, and a paucity of empirical information often leads to inconsistent definitions of trophic guilds based on expert opinion, especially when applied to hyperdiverse ecosystems. Using coral reef fishes as a model group, we show that experts disagree on the assignment of broad trophic guilds for more than 20% of species, which hampers comparability across studies. Here, we propose a quantitative, unbiased, and reproducible approach to define trophic guilds and apply recent advances in machine learning to predict probabilities of pairwise trophic interactions with high accuracy. We synthesize data from community-wide gut content analyses of tropical coral reef fishes worldwide, resulting in diet information from 13,961 individuals belonging to 615 reef fish. We then use network analysis to identify 8 trophic guilds and Bayesian phylogenetic modeling to show that trophic guilds can be predicted based on phylogeny and maximum body size. Finally, we use machine learning to test whether pairwise trophic interactions can be predicted with accuracy. Our models achieved a misclassification error of less than 5%, indicating that our approach results in a quantitative and reproducible trophic categorization scheme, as well as high-resolution probabilities of trophic interactions. By applying our framework to the most diverse vertebrate consumer group, we show that it can be applied to other organismal groups to advance reproducibility in trait-based ecology. Our work thus provides a viable approach to account for the complexity of predator-prey interactions in highly diverse ecosystems.

Effects of the COVID-19 lockdowns on the management of coral restoration projects.

Coral restoration initiatives are gaining significant momentum in a global effort to enhance the recovery of degraded coral reefs. However, the implementation and upkeep of coral nurseries are particularly demanding, so that unforeseen breaks in maintenance operations might jeopardize well-established projects. In the last 2 years, the COVID-19 pandemic has resulted in a temporary yet prolonged abandonment of several coral gardening infrastructures worldwide, including remote localities. Here we provide a first assessment of the potential impacts of monitoring and maintenance breakdown in a suite of coral restoration projects (based on floating rope nurseries) in Colombia, Seychelles, and Maldives. Our study comprises nine nurseries from six locations, hosting a total of 3,554 fragments belonging to three coral genera, that were left unsupervised for a period spanning from 29 to 61 weeks. Floating nursery structures experienced various levels of damage, and total fragment survival spanned from 40 to 95% among projects, with Pocillopora showing the highest survival rate in all locations present. Overall, our study shows that, under certain conditions, abandoned coral nurseries can remain functional for several months without suffering critical failure from biofouling and hydrodynamism. Still, even where gardening infrastructures were only marginally affected, the unavoidable interruptions in data collection have slowed down ongoing project progress, diminishing previous investments and reducing future funding opportunities. These results highlight the need to increase the resilience and self-sufficiency of coral restoration projects, so that the next global lockdown will not further shrink the increasing efforts to prevent coral reefs from disappearing.

Global tropical reef fish richness could decline by around half if corals are lost.

Reef fishes are a treasured part of marine biodiversity, and also provide needed protein for many millions of people. Although most reef fishes might survive projected increases in ocean temperatures, corals are less tolerant. A few fish species strictly depend on corals for food and shelter, suggesting that coral extinctions could lead to some secondary fish extinctions. However, secondary extinctions could extend far beyond those few coral-dependent species. Furthermore, it is yet unknown how such fish declines might vary around the world. Current coral mass mortalities led us to ask how fish communities would respond to coral loss within and across oceans. We mapped 6964 coral-reef-fish species and 119 coral genera, and then regressed reef-fish species richness against coral generic richness at the 1° scale (after controlling for biogeographic factors that drive species diversification). Consistent with small-scale studies, statistical extrapolations suggested that local fish richness across the globe would be around half its current value in a hypothetical world without coral, leading to more areas with low or intermediate fish species richness and fewer fish diversity hotspots.

Small room for compromise between oil palm cultivation and primate conservation in Africa.

Despite growing awareness about its detrimental effects on tropical biodiversity, land conversion to oil palm continues to increase rapidly as a consequence of global demand, profitability, and the income opportunity it offers to producing countries. Although most industrial oil palm plantations are located in Southeast Asia, it is argued that much of their future expansion will occur in Africa. We assessed how this could affect the continent's primates by combining information on oil palm suitability and current land use with primate distribution, diversity, and vulnerability. We also quantified the potential impact of large-scale oil palm cultivation on primates in terms of range loss under different expansion scenarios taking into account future demand, oil palm suitability, human accessibility, carbon stock, and primate vulnerability. We found a high overlap between areas of high oil palm suitability and areas of high conservation priority for primates. Overall, we found only a few small areas where oil palm could be cultivated in Africa with a low impact on primates (3.3 Mha, including all areas suitable for oil palm). These results warn that, consistent with the dramatic effects of palm oil cultivation on biodiversity in Southeast Asia, reconciling a large-scale development of oil palm in Africa with primate conservation will be a great challenge.

Bi-dimensional null model analysis of presence-absence binary matrices.

Comparing the structure of presence/absence (i.e., binary) matrices with those of randomized counterparts is a common practice in ecology. However, differences in the randomization procedures (null models) can affect the results of the comparisons, leading matrix structural patterns to appear either "random" or not. Subjectivity in the choice of one particular null model over another makes it often advisable to compare the results obtained using several different approaches. Yet, available algorithms to randomize binary matrices differ substantially in respect to the constraints they impose on the discrepancy between observed and randomized row and column marginal totals, which complicates the interpretation of contrasting patterns. This calls for new strategies both to explore intermediate scenarios of restrictiveness in-between extreme constraint assumptions, and to properly synthesize the resulting information. Here we introduce a new modeling framework based on a flexible matrix randomization algorithm (named the "Tuning Peg" algorithm) that addresses both issues. The algorithm consists of a modified swap procedure in which the discrepancy between the row and column marginal totals of the target matrix and those of its randomized counterpart can be "tuned" in a continuous way by two parameters (controlling, respectively, row and column discrepancy). We show how combining the Tuning Peg with a wise random walk procedure makes it possible to explore the complete null space embraced by existing algorithms. This exploration allows researchers to visualize matrix structural patterns in an innovative bi-dimensional landscape of significance/effect size. We demonstrate the rational and potential of our approach with a set of simulated and real matrices, showing how the simultaneous investigation of a comprehensive and continuous portion of the null space can be extremely informative, and possibly key to resolving longstanding debates in the analysis of ecological matrices.

Monitoring and assessing a 2-year outbreak of the corallivorous seastar Acanthaster planci in Ari Atoll, Republic of Maldives.

Outbreaks of the corallivorous crown-of-thorns seastars have received increasing attention due to their negative impacts on coral reefs in the Indo-Pacific Ocean. However, outbreaks in remote and dislocated islands are still poorly understood. This study aims to begin filling informational gaps regarding outbreaks of Acanthaster planci in the remote islands of the central Ari Atoll, Republic of Maldives. The population of A. planci was monitored during three periods over 2 years (2015-2016) to evaluate variations in abundance and to characterise size structure and feeding behaviour. The outbreak appeared to be severe and active throughout the entire study period. The size structure analysis revealed a multimodal distribution dominated by individuals between 20 and 30 cm, suggesting that the outbreak may have resulted from a few nearby mass spawning events. Additionally, the most abundant live coral was Porites, which was also the most consumed genus; however, the electivity index showed a preference for corals of the genera Favites and Pavona. Finally, we also highlighted the need for more geographically extended surveys to better understand local patterns regarding outbreaks of A. planci in the Republic of Maldives.

Corals hosting symbiotic hydrozoans are less susceptible to predation and disease.

In spite of growing evidence that climate change may dramatically affect networks of interacting species, whether-and to what extent-ecological interactions can mediate species' responses to disturbances is an open question. Here we show how a largely overseen association such as that between hydrozoans and scleractinian corals could be possibly associated with a reduction in coral susceptibility to ever-increasing predator and disease outbreaks. We examined 2455 scleractinian colonies (from both Maldivian and the Saudi Arabian coral reefs) searching for non-random patterns in the occurrence of hydrozoans on corals showing signs of different health conditions (i.e. bleaching, algal overgrowth, corallivory and different coral diseases). We show that, after accounting for geographical, ecological and co-evolutionary factors, signs of disease and corallivory are significantly lower in coral colonies hosting hydrozoans than in hydrozoan-free ones. This finding has important implications for our understanding of the ecology of coral reefs, and for their conservation in the current scenario of global change, because it suggests that symbiotic hydrozoans may play an active role in protecting their scleractinian hosts from stresses induced by warming water temperatures.

Are generalist parasites being lost from their hosts?

Co-extinctions should be regarded as fundamental co-evolutionary events promoting species turnover, prior than a consequence of human induced biodiversity loss. Focusing on current scenarios is key to biodiversity conservation, but predicting future trends could be harder and less fruitful than trying to get a better grasp on the past.

Projected loss of brown macroalgae and seagrasses with global environmental change.

Although many studies predict extensive future biodiversity loss and redistribution in the terrestrial realm, future changes in marine biodiversity remain relatively unexplored. In this work, we model global shifts in one of the most important marine functional groups-ecosystem-structuring macrophytes-and predict substantial end-of-century change. By modelling the future distribution of 207 brown macroalgae and seagrass species at high temporal and spatial resolution under different climate-change projections, we estimate that by 2100, local macrophyte diversity will decline by 3-4% on average, with 17 to 22% of localities losing at least 10% of their macrophyte species. The current range of macrophytes will be eroded by 5-6%, and highly suitable macrophyte habitat will be substantially reduced globally (78-96%). Global macrophyte habitat will shift among marine regions, with a high potential for expansion in polar regions.

Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

Prevalence, host range, and spatial distribution of black band disease in the Maldivian Archipelago.

Little research has been conducted on diseases affecting reef-building corals in the central Indian Ocean. During 2010 and 2011, we performed a quantitative assessment of black band disease (BBD) in the central Republic of Maldives. Distribution, host range, and prevalence of BBD were investigated at 6 coral islands (Magoodhoo, Adanga, Ihuru, Vabbinfaru, Thudufushi, and Athuruga) belonging to 3 different atolls. BBD was found to be widespread among the atolls. All the islands showed a prevalence lower than 0.5%. Magoodhoo Island showed the highest mean disease prevalence. In the whole surveyed area, shallow sites showed higher overall mean BBD prevalence than deep ones. BBD was recorded from 6 scleractinian families (Acroporidae, Faviidae, Poritidae, Siderastreidae, Agariciidae, Fungiidae) and 13 scleractinian genera. Two of them, Gardineroseris and Sandalolitha, constitute new records for the disease. The siderastreid Psammocora (BBD prevalence: 5.33 ± 1.41%, mean ± SE) was the most affected genus, followed by Goniopora (2.7 ± 1.3%). BBD prevalence was positively correlated to the respective host density in both genera. Favites and Acropora were the less affected genera (both <0.1%). Although we observed an extremely low overall disease prevalence in the surveyed area (<1%), the large number of different scleractinian genera affected and the widespread distribution of BBD indicate a need for further investigation.

First report of coral diseases in the Republic of Maldives.

Little is known about coral diseases in the Indian Ocean region, especially in the Republic of Maldives. This study aimed at documenting the presence of coral diseases in the archipelago of the Maldives. Surveys for lesions in scleractinians conducted at 8 sites around Magoodhoo Island (Faafu Atoll) in October and November 2010 led to the identification of 5 coral diseases and 1 anomalous pigmentation response affecting 8 hard coral genera. White syndrome, skeleton-eroding band disease, black band disease, and Porites dark discoloration response were the most commonly observed conditions. In contrast with several reports of other reef systems, the overall observed prevalence of coral diseases was rather low (<2%), with individual prevalence ranging from 0.7% for skeleton-eroding band to 0.18% for Porites dark discoloration response. These data represent the first report of coral diseases for the Republic of Maldives.

A patch-dynamic metacommunity perspective on the persistence of mutualistic and antagonistic bipartite networks.

The structure of interactions between species within a community plays a key role in maintaining biodiversity. Previous studies found that the effects of these structures might vary substantially depending on interaction type, for example, a highly connected and nested architecture stabilizes mutualistic communities, while the stability of antagonistic communities is enhanced in modular and weakly connected structures. Here we show that, when network dynamics are modeled using a patch-dynamic metacommunity framework, the qualitative differences between antagonistic and mutualistic systems disappear, with nestedness and modularity interacting to promote metacommunity persistence. However, the interactive effects are significantly weaker in antagonistic metacommunities. Our model also predicts an increase in connectance, nestedness, and modularity over time in both types of interaction, except in antagonistic networks, where nestedness declines. At steady state, we find a strong negative correlation between nestedness and modularity in both mutualistic and antagonistic metacommunities. These predictions are consistent with the structural trends found in a large data set of real-world antagonistic and mutualistic communities.

Coextinctions dominate future vertebrate losses from climate and land use change.

Although theory identifies coextinctions as a main driver of biodiversity loss, their role at the planetary scale has yet to be estimated. We subjected a global model of interconnected terrestrial vertebrate food webs to future (2020-2100) climate and land-use changes. We predict a 17.6% (± 0.16% SE) average reduction of local vertebrate diversity globally by 2100, with coextinctions increasing the effect of primary extinctions by 184.2% (± 10.9% SE) on average under an intermediate emissions scenario. Communities will lose up to a half of ecological interactions, thus reducing trophic complexity, network connectance, and community resilience. The model reveals that the extreme toll of global change for vertebrate diversity might be of secondary importance compared to the damages to ecological network structure.

Unveiling the complexity and ecological function of aquatic macrophyte-animal networks in coastal ecosystems.

Network theory offers innovative tools to explore the complex ecological mechanisms regulating species associations and interactions. Although interest in ecological networks has grown steadily during the last two decades, the application of network approaches has been unequally distributed across different study systems: while some kinds of interactions (e.g. plant-pollinator and host-parasite) have been extensively investigated, others remain relatively unexplored. Among the latter, aquatic macrophyte-animal associations in coastal environments have been largely neglected, despite their major role in littoral ecosystems. The ubiquity of macrophyte systems, their accessibility and multi-faceted ecological, economical and societal importance make macrophyte-animal systems an ideal subject for ecological network science. In fact, macrophyte-animal networks offer an aquatic counterpart to terrestrial plant-animal networks. In this review, we show how the application of network analysis to aquatic macrophyte-animal associations has the potential to broaden our understanding of how coastal ecosystems function. Network analysis can also provide a key to understanding how such ecosystems will respond to on-going and future threats from anthropogenic disturbance and environmental change. For this, we: (i) identify key issues that have limited the application of network theory and modelling to aquatic animal-macrophyte associations; (ii) illustrate through examples based on empirical data how network analysis can offer new insights on the complexity and functioning of coastal ecosystems; and (iii) provide suggestions for how to design future studies and establish this new research line into network ecology.