Modeling time-varying phytoplankton subsidy reveals at-risk species in a Chilean intertidal ecosystem.

The allometric trophic network (ATN) framework for modeling population dynamics has provided numerous insights into ecosystem functioning in recent years. Herein we extend ATN modeling of the intertidal ecosystem off central Chile to include empirical data on pelagic chlorophyll-a concentration. This intertidal community requires subsidy of primary productivity to support its rich ecosystem. Previous work models this subsidy using a constant rate of phytoplankton input to the system. However, data shows pelagic subsidies exhibit highly variable, pulse-like behavior. The primary contribution of our work is incorporating this variable input into ATN modeling to simulate how this ecosystem may respond to pulses of pelagic phytoplankton. Our model results show that: (1) closely related sea snails respond differently to phytoplankton variability, which is explained by the underlying network structure of the food web; (2) increasing the rate of pelagic-intertidal mixing increases fluctuations in species' biomasses that may increase the risk of local extirpation; (3) predators are the most sensitive species to phytoplankton biomass fluctuations, putting these species at greater risk of extirpation than others. Finally, our work provides a straightforward way to incorporate empirical, time-series data into the ATN framework that will expand this powerful methodology to new applications.

Emergent Spatial Patterns Can Indicate Upcoming Regime Shifts in a Realistic Model of Coral Community.

AbstractIncreased stress on coastal ecosystems, such as coral reefs, seagrasses, kelp forests, and other habitats, can make them shift toward degraded, often algae-dominated or barren communities. This has already occurred in many places around the world, calling for new approaches to identify where such regime shifts may be triggered. Theoretical work predicts that the spatial structure of habitat-forming species should exhibit changes prior to regime shifts, such as an increase in spatial autocorrelation. However, extending this theory to marine systems requires theoretical models connecting field-supported ecological mechanisms to data and spatial patterns at relevant scales. To do so, we built a spatially explicit model of subtropical coral communities based on experiments and long-term datasets from Rapa Nui (Easter Island, Chile), to test whether spatial indicators could signal upcoming regime shifts in coral communities. Spatial indicators anticipated degradation of coral communities following increases in frequency of bleaching events or coral mortality. However, they were generally unable to signal shifts that followed herbivore loss, a widespread and well-researched source of degradation, likely because herbivory, despite being critical for the maintenance of corals, had comparatively little effect on their self-organization. Informative trends were found under both equilibrium and nonequilibrium conditions but were determined by the type of direct neighbor interactions between corals, which remain relatively poorly documented. These inconsistencies show that while this approach is promising, its application to marine systems will require detailed information about the type of stressor and filling current gaps in our knowledge of interactions at play in coral communities.

Environmental DNA reveals temporal variation in mesophotic reefs of the Humboldt upwelling ecosystems of central Chile: Toward a baseline for biodiversity monitoring of unexplored marine habitats.

Temperate mesophotic reef ecosystems (TMREs) are among the least known marine habitats. Information on their diversity and ecology is geographically and temporally scarce, especially in highly productive large upwelling ecosystems. Lack of information remains an obstacle to understanding the importance of TMREs as habitats, biodiversity reservoirs and their connections with better-studied shallow reefs. Here, we use environmental DNA (eDNA) from water samples to characterize the community composition of TMREs on the central Chilean coast, generating the first baseline for monitoring the biodiversity of these habitats. We analyzed samples from two depths (30 and 60 m) over four seasons (spring, summer, autumn, and winter) and at two locations approximately 16 km apart. We used a panel of three metabarcodes, two that target all eukaryotes (18S rRNA and mitochondrial COI) and one specifically targeting fishes (16S rRNA). All panels combined encompassed eDNA assigned to 42 phyla, 90 classes, 237 orders, and 402 families. The highest family richness was found for the phyla Arthropoda, Bacillariophyta, and Chordata. Overall, family richness was similar between depths but decreased during summer, a pattern consistent at both locations. Our results indicate that the structure (composition) of the mesophotic communities varied predominantly with seasons. We analyzed further the better-resolved fish assemblage and compared eDNA with other visual methods at the same locations and depths. We recovered eDNA from 19 genera of fish, six of these have also been observed on towed underwater videos, while 13 were unique to eDNA. We discuss the potential drivers of seasonal differences in community composition and richness. Our results suggest that eDNA can provide valuable insights for monitoring TMRE communities but highlight the necessity of completing reference DNA databases available for this region.

Spatio-temporal patterns of the crustacean demersal fishery discard from the south Humboldt Current System, based on scientific observer program (2014-2019).

This study summarises six years of spatio-temporal patterns of the discarded demersal community fauna recorded by onboard scientific observer program for both artisanal and industrial crustacean fisheries between 2014 and 2019, from mesophotic to aphotic depths (96 to 650 m) along the southern Humboldt Current System (28-38°S). In this period, one cold and two warm climatic events were observed during the austral summer 2014, 2015-2016 (ENSO Godzilla), and 2016-2017 (coastal ENSO), respectively. Satellite information showed that Chlorophyll-a concentration varied seasonally and latitudinally, associated with upwelling centres, while equatorial wind stress decreased southward of 36°S. Discards were composed of 108 species, dominated by finfish and molluscs. The Chilean hake Merluccius gayi was dominant and ubiquitous (occurrence, 95% of 9104 hauls), being the most vulnerable species of the bycatch. Three assemblages were identified: assemblage 1 (~200 m deep), dominated by flounders Hippoglossina macrops and lemon crabs Platymera gaudichaudii, assemblage 2 (~260 m deep), dominated by squat lobsters Pleuroncodes monodon and Cervimunida johni and assemblage 3 (~320 m depth), dominated by grenadiers Coelorinchus aconcagua and cardinalfish Epigonus crassicaudus. These assemblages were segregated by depth, and varied by year, and geographic zone. The latter represented changes in the width of the continental shelf, increasing southward of 36°S. Alpha-diversity indexes (richness, Shannon, Simpson, and Pielou) also varied with depth and latitude, with higher diversity in deeper continental waters (>300 m), between 2018-2019. Finally, at a spatial scale of tens of kilometres, and a monthly basis, interannual variations of biodiversity occurred in the demersal community. Surface sea temperature, chlorophyll-a, or wind stress did not correlate with discarded demersal fauna diversity of the crustacean fishery operating along central Chile.

Alteration of coastal productivity and artisanal fisheries interact to affect a marine food web.

Top-down and bottom-up forces determine ecosystem function and dynamics. Fisheries as a top-down force can shorten and destabilize food webs, while effects driven by climate change can alter the bottom-up forces of primary productivity. We assessed the response of a highly-resolved intertidal food web to these two global change drivers, using network analysis and bioenergetic modelling. We quantified the relative importance of artisanal fisheries as another predator species, and evaluated the independent and combined effects of fisheries and changes in plankton productivity on food web dynamics. The food web was robust to the loss of all harvested species but sensitive to the decline in plankton productivity. Interestingly, fisheries dampened the negative impacts of decreasing plankton productivity on non-harvested species by reducing the predation pressure of harvested consumers on non-harvested resources, and reducing the interspecific competition between harvested and non-harvested basal species. In contrast, the decline in plankton productivity increased the sensitivity of harvested species to fishing by reducing the total productivity of the food web. Our results show that strategies for new scenarios caused by climate change are needed to protect marine ecosystems and the wellbeing of local communities dependent on their resources.

Geographical variation of multiplex ecological networks in marine intertidal communities.

Understanding the drivers of geographical variation in species distributions, and the resulting community structure, constitutes one of the grandest challenges in ecology. Geographical patterns of species richness and composition have been relatively well studied. Less is known about how the entire set of trophic and non-trophic ecological interactions, and the complex networks that they create by gluing species together in complex communities, change across geographical extents. Here, we compiled data of species composition and three types of ecological interactions occurring between species in rocky intertidal communities across a large spatial extent (~970 km of shoreline) of central Chile, and analyzed the geographical variability in these multiplex networks (i.e., comprising several interaction types) of ecological interactions. We calculated nine network summary statistics common across interaction types, and additional network attributes specific to each of the different types of interactions. We then investigated potential environmental drivers of this multivariate network organization. These included variation in sea surface temperature and coastal upwelling, the main drivers of productivity in nearshore waters. Our results suggest that structural properties of multiplex ecological networks are affected by local species richness and modulated by factors influencing productivity and environmental predictability. Our results show that non-trophic negative interactions are more sensitive to spatially structured temporal environmental variation than feeding relationships, with non-trophic positive interactions being the least labile to it. We also show that environmental effects are partly mediated through changes in species richness and partly through direct influences on species interactions, probably associated to changes in environmental predictability and to bottom-up nutrient availability. Our findings highlight the need for a comprehensive picture of ecological interactions and their geographical variability if we are to predict potential effects of environmental changes on ecological communities.

Removal of intertidal grazers by human harvesting leads to alteration of species interactions, community structure and resilience to climate change.

Extreme fluctuations in abiotic conditions can induce a biological stress response (e.g. bleaching) detrimental to an organism's health. In some instances, organisms can recover if conditions are alleviated, such as through co-occurrence with other species that confer protection. Biodiverse, multitrophic communities are increasingly recognised as important promoters of species persistence and resilience under environmental change. On intertidal shores, the role of grazers as top-down determinants of algal community structure is well recognised. Similarly, the harvesting of grazers for human consumption is increasingly prevalent with potential to greatly alter the community dynamics. Here, we assess how differences in harvesting pressure of grazers under three management regimes (no-take; managed access; open-access) alters the trophic interactions between grazers, and algal communities. Grazer density and body size frequencies were different among regimes leading to changes in the photosynthetic performance and recovery of crustose coralline algae (CCA) post-bleaching, as well as their presence altering the strength of interactions between species. The exclusion of grazers from patches using cages led to different emergent communities and reduced negative correlations between taxa. The absence of larger grazers (>9 cm) at the managed access site led to macroalgal overgrowth of bleached CCA negatively affecting its recovery, whereas no-take or open-access led to a moderated algal growth and a shift from competitive to facilitative interactions between algal species. Given that CCA play an important role in the population growth and development of other species, the choice of management measure should be carefully considered before implementation, depending on objectives.

Species co-occurrence networks: Can they reveal trophic and non-trophic interactions in ecological communities?

Co-occurrence methods are increasingly utilized in ecology to infer networks of species interactions where detailed knowledge based on empirical studies is difficult to obtain. Their use is particularly common, but not restricted to, microbial networks constructed from metagenomic analyses. In this study, we test the efficacy of this procedure by comparing an inferred network constructed using spatially intensive co-occurrence data from the rocky intertidal zone in central Chile to a well-resolved, empirically based, species interaction network from the same region. We evaluated the overlap in the information provided by each network and the extent to which there is a bias for co-occurrence data to better detect known trophic or non-trophic, positive or negative interactions. We found a poor correspondence between the co-occurrence network and the known species interactions with overall sensitivity (probability of true link detection) equal to 0.469, and specificity (true non-interaction) equal to 0.527. The ability to detect interactions varied with interaction type. Positive non-trophic interactions such as commensalism and facilitation were detected at the highest rates. These results demonstrate that co-occurrence networks do not represent classical ecological networks in which interactions are defined by direct observations or experimental manipulations. Co-occurrence networks provide information about the joint spatial effects of environmental conditions, recruitment, and, to some extent, biotic interactions, and among the latter, they tend to better detect niche-expanding positive non-trophic interactions. Detection of links (sensitivity or specificity) was not higher for well-known intertidal keystone species than for the rest of consumers in the community. Thus, as observed in previous empirical and theoretical studies, patterns of interactions in co-occurrence networks must be interpreted with caution, especially when extending interaction-based ecological theory to interpret network variability and stability. Co-occurrence networks may be particularly valuable for analysis of community dynamics that blends interactions and environment, rather than pairwise interactions alone.

How Structured Is the Entangled Bank? The Surprisingly Simple Organization of Multiplex Ecological Networks Leads to Increased Persistence and Resilience.

Species are linked to each other by a myriad of positive and negative interactions. This complex spectrum of interactions constitutes a network of links that mediates ecological communities' response to perturbations, such as exploitation and climate change. In the last decades, there have been great advances in the study of intricate ecological networks. We have, nonetheless, lacked both the data and the tools to more rigorously understand the patterning of multiple interaction types between species (i.e., "multiplex networks"), as well as their consequences for community dynamics. Using network statistical modeling applied to a comprehensive ecological network, which includes trophic and diverse non-trophic links, we provide a first glimpse at what the full "entangled bank" of species looks like. The community exhibits clear multidimensional structure, which is taxonomically coherent and broadly predictable from species traits. Moreover, dynamic simulations suggest that this non-random patterning of how diverse non-trophic interactions map onto the food web could allow for higher species persistence and higher total biomass than expected by chance and tends to promote a higher robustness to extinctions.

Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores.

How multiple types of non-trophic interactions map onto trophic networks in real communities remains largely unknown. We present the first effort, to our knowledge, describing a comprehensive ecological network that includes all known trophic and diverse non-trophic links among >100 coexisting species for the marine rocky intertidal community of the central Chilean coast. Our results suggest that non-trophic interactions exhibit highly nonrandom structures both alone and with respect to food web structure. The occurrence of different types of interactions, relative to all possible links, was well predicted by trophic structure and simple traits of the source and target species. In this community, competition for space and positive interactions related to habitat/refuge provisioning by sessile and/or basal species were by far the most abundant non-trophic interactions. If these patterns are orroborated in other ecosystems, they may suggest potentially important dynamic constraints on the combined architecture of trophic and non-trophic interactions. The nonrandom patterning of non-trophic interactions suggests a path forward for developing a more comprehensive ecological network theory to predict the functioning and resilience of ecological communities.

Latitudinal discontinuity in thermal conditions along the nearshore of central-northern Chile.

Over the past decade, evidence of abrupt latitudinal changes in the dynamics, structure and genetic variability of intertidal and subtidal benthic communities along central-northern Chile has been found consistently at 30-32°S. Changes in the advective and thermal environment in nearshore waters have been inferred from ecological patterns, since analyses of in situ physical data have thus far been missing. Here we analyze a unique set of shoreline temperature data, gathered over 4-10 years at 15 sites between 28-35°S, and combine it with satellite-derived winds and sea surface temperatures to investigate the latitudinal transition in nearshore oceanographic conditions suggested by recent ecological studies. Our results show a marked transition in thermal conditions at 30-31°S, superimposed on a broad latitudinal trend, and small-scale structures associated with cape-and-bay topography. The seasonal cycle dominated temperature variability throughout the region, but its relative importance decreased abruptly south of 30-31°S, as variability at synoptic and intra-seasonal scales became more important. The response of shoreline temperatures to meridional wind stress also changed abruptly at the transition, leading to a sharp drop in the occurrence of low-temperature waters at northern sites, and a concurrent decrease in corticated algal biomass. Together, these results suggest a limitation of nitrate availability in nearshore waters north of the transition. The localized alongshore change results from the interaction of latitudinal trends (e.g., wind stress, surface warming, inertial period) with a major headland-bay system (Punta Lengua de Vaca at 30.25°S), which juxtaposes a southern stretch of coast characterized by upwelling with a northern stretch of coast characterized by warm surface waters and stratification. This transition likely generates a number of latitude-dependent controls on ecological processes in the nearshore that can explain species-specific effects, and add strength to the suggestion of an oceanography-driven, major spatial transition in coastal communities at 30-31°S.

Biogeographical boundaries, functional group structure and diversity of Rocky Shore communities along the Argentinean coast.

We investigate the extent to which functional structure and spatial variability of intertidal communities coincide with major biogeographical boundaries, areas where extensive compositional changes in the biota are observed over a limited geographic extension. We then investigate whether spatial variation in the biomass of functional groups, over geographic (10's km) and local (10's m) scales, could be associated to species diversity within and among these groups. Functional community structure expressed as abundance (density, cover and biomass) and composition of major functional groups was quantified through field surveys at 20 rocky intertidal shores spanning six degrees of latitude along the southwest Atlantic coast of Argentina and extending across the boundaries between the Argentinean and Magellanic Provinces. Patterns of abundance of individual functional groups were not uniformly matched with biogeographical regions. Only ephemeral algae showed an abrupt geographical discontinuity coincident with changes in biogeographic boundaries, and this was limited to the mid intertidal zone. We identified 3-4 main 'groups' of sites in terms of the total and relative abundance of the major functional groups, but these did not coincide with biogeographical boundaries, nor did they follow latitudinal arrangement. Thus, processes that determine the functional structure of these intertidal communities are insensitive to biogeographical boundaries. Over both geographical and local spatial scales, and for most functional groups and tidal levels, increases in species richness within the functional group was significantly associated to increased total biomass and reduced spatial variability of the group. These results suggest that species belonging to the same functional group are sufficiently uncorrelated over space (i.e. metres and site-to-site ) to stabilize patterns of biomass variability and, in this manner, provide a buffer, or "insurance", against spatial variability in environmental conditions.

More than a meal integrating non-feeding interactions into food webs.

Organisms eating each other are only one of many types of well documented and important interactions among species. Other such types include habitat modification, predator interference and facilitation. However, ecological network research has been typically limited to either pure food webs or to networks of only a few (<3) interaction types. The great diversity of non-trophic interactions observed in nature has been poorly addressed by ecologists and largely excluded from network theory. Herein, we propose a conceptual framework that organises this diversity into three main functional classes defined by how they modify specific parameters in a dynamic food web model. This approach provides a path forward for incorporating non-trophic interactions in traditional food web models and offers a new perspective on tackling ecological complexity that should stimulate both theoretical and empirical approaches to understanding the patterns and dynamics of diverse species interactions in nature.

Scales of dispersal and the biogeography of marine predator-prey interactions.

Striking differences in the dispersal of coexisting species have fascinated marine ecologists for decades. Despite widespread attention to the impact of dispersal on individual species dynamics, its role in species interactions has received comparatively little attention. Here, we approach the issue by combining analyses of simple heuristic predator-prey models with different dispersal patterns and data from several predator-prey systems from the Pacific coasts of North and South America. In agreement with model predictions, differences in predator dispersal generated characteristic biogeographic patterns. Predators lacking pelagic larvae tracked geographic variation in prey recruitment but not prey abundance. Prey recruitment rate alone explained more than 80% of the biogeographic variation in predator abundance. In contrast, predators with broadcasting larvae were uncorrelated with prey recruitment or adult prey abundance. Our findings reconcile perplexing results from previous studies and suggest that simple models can capture some of the complexity of life-history diversity in marine communities.

Scales of benthic-pelagic coupling and the intensity of species interactions: from recruitment limitation to top-down control.

Large and usually unpredictable variation in species interaction strength has been a major roadblock to applying local experimental results to large-scale management and conservation issues. Recent studies explicitly considering benthic-pelagic coupling are starting to shed light on, and find regularities in, the causes of such large-scale variation in coastal ecosystems. Here, we evaluate the effects of variation in wind-driven upwelling on community regulation along 900 km of coastline of the southeastern Pacific, between 29 degrees S and 35 degrees S during 72 months. Variability in the intensity of upwelling occurring over tens of km produced predictable variation in recruitment of intertidal mussels, but not barnacles, and did not affect patterns of community structure. In contrast, sharp discontinuities in upwelling regimes produced abrupt and persistent breaks in the dynamics of benthic and pelagic communities over hundreds of km (regional) scales. Rates of mussel and barnacle recruitment changed sharply at approximately 32 degrees -33 degrees S, determining a geographic break in adult abundance of these competitively dominant species. Analysis of satellite images demonstrates that regional-scale discontinuities in oceanographic regimes can couple benthic and pelagic systems, as evidenced by coincident breaks in dynamics and concentration of offshore surface chlorophyll-a. Field experiments showed that the paradigm of top-down control of intertidal benthic communities holds only south of the discontinuity. To the north, populations seem recruitment-limited, and predators have negligible effects, despite attaining similarly high abundances and potential predation effects across the region. Thus, geographically discontinuous oceanographic regimes set bounds to the strength of species interactions and define distinct regions for the design and implementation of sustainable management and conservation policies.