Landscape fragmentation overturns classical metapopulation thinking.

Habitat loss and isolation caused by landscape fragmentation represent a growing threat to global biodiversity. Existing theory suggests that the process will lead to a decline in metapopulation viability. However, since most metapopulation models are restricted to simple networks of discrete habitat patches, the effects of real landscape fragmentation, particularly in stochastic environments, are not well understood. To close this major gap in ecological theory, we developed a spatially explicit, individual-based model applicable to realistic landscape structures, bridging metapopulation ecology and landscape ecology. This model reproduced classical metapopulation dynamics under conventional model assumptions, but on fragmented landscapes, it uncovered general dynamics that are in stark contradiction to the prevailing views in the ecological and conservation literature. Notably, fragmentation can give rise to a series of dualities: a) positive and negative responses to environmental noise, b) relative slowdown and acceleration in density decline, and c) synchronization and desynchronization of local population dynamics. Furthermore, counter to common intuition, species that interact locally ("residents") were often more resilient to fragmentation than long-ranging "migrants." This set of findings signals a need to fundamentally reconsider our approach to ecosystem management in a noisy and fragmented world.

The chytrid insurance hypothesis: integrating parasitic chytrids into a biodiversity-ecosystem functioning framework for phytoplankton-zooplankton population dynamics.

In temperate lakes, eutrophication and warm temperatures can promote cyanobacteria blooms that reduce water quality and impair food-chain support. Although parasitic chytrids of phytoplankton might compete with zooplankton, they also indirectly support zooplankton populations through the "mycoloop", which helps move energy and essential dietary molecules from inedible phytoplankton to zooplankton. Here, we consider how the mycoloop might fit into the biodiversity-ecosystem functioning (BEF) framework. BEF considers how more diverse communities can benefit ecosystem functions like zooplankton production. Chytrids are themselves part of pelagic food webs and they directly contribute to zooplankton diets through spore production and by increasing host edibility. The additional way that chytrids might support BEF is if they engage in "kill-the-winner" dynamics. In contrast to grazers, which result in "eat-the-edible" dynamics, kill-the-winner dynamics can occur for host-specific infectious diseases that control the abundance of dominant (in this case inedible) hosts and thus limit the competitive exclusion of poorer (in this case edible) competitors. Thus, if phytoplankton diversity provides functions, and chytrids support algal diversity, chytrids could indirectly favour edible phytoplankton. All three mechanisms are linked to diversity and therefore provide some "insurance" for zooplankton production against the impacts of eutrophication and warming. In our perspective piece, we explore evidence for the chytrid insurance hypothesis, identify exceptions and knowledge gaps, and outline future research directions.

Parasites alter food-web topology of a subarctic lake food web and its pelagic and benthic compartments.

We compared three sets of highly resolved food webs with and without parasites for a subarctic lake system corresponding to its pelagic and benthic compartments and the whole-lake food web. Key topological food-web metrics were calculated for each set of compartments to explore the role parasites play in food-web topology in these highly contrasting webs. After controlling for effects from differences in web size, we observed similar responses to the addition of parasites in both the pelagic and benthic compartments demonstrated by increases in trophic levels, linkage density, connectance, generality, and vulnerability despite the contrasting composition of free-living and parasitic species between the two compartments. Similar effects on food-web topology can be expected with the inclusion of parasites, regardless of the physical characteristics and taxonomic community compositions of contrasting environments. Additionally, similar increases in key topological metrics were found in the whole-lake food web that combines the pelagic and benthic webs, effects that are comparable to parasite food-web analyses from other systems. These changes in topological metrics are a result of the unique properties of parasites as infectious agents and the links they participate in. Trematodes were key contributors to these results, as these parasites have distinct characteristics in aquatic systems that introduce new link types and increase the food web's generality and vulnerability disproportionate to other parasites. Our analysis highlights the importance of incorporating parasites, especially trophically transmitted parasites, into food webs as they significantly alter key topological metrics and are thus essential for understanding an ecosystem's structure and functioning.

Parasites in kelp-forest food webs increase food-chain length, complexity, and specialization, but reduce connectance.

We explored whether parasites are important in kelp forests by examining their effects on a high-quality, high-resolution kelp-forest food web. After controlling for generic effects of network size, parasites affected kelp-forest food web structure in some ways consistent with other systems. Parasites increased the trophic span of the web, increasing top predator vulnerability and the longest chain length. Unique links associated with parasites, such as concomitant predation (consumption of parasites along with their hosts by predators) increased the frequency of network motifs involving mutual consumption and decreased niche contiguity of free-living species. However, parasites also affected kelp-forest food web structure in ways not seen in other systems. Kelp-forest parasites are richer and more specialized than other systems. As a result, parasites reduced diet generality and decreased connectance in the kelp forest. Although mutual consumption motifs increased in frequency, this motif type was still a small fraction of all possible motifs, so their increase in frequency was not enough to compensate for the decrease in connectance caused by adding many specialist parasite species.

Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission.

Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.

Trade-Offs with Growth Limit Host Range in Complex Life-Cycle Helminths.

AbstractParasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a data set for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we confirmed that worms with longer life cycles (i.e., more successive hosts) infect a greater diversity of host species and taxa (after controlling for study effort). Generalism at the stage level was highest for middle life stages, the second and third intermediate hosts of long life cycles. By simulating life cycles in real food webs, we found that middle stages had more potential host species to infect, suggesting that opportunity constrains generalism. However, parasites usually infected fewer host species than expected from simulated cycles, suggesting that generalism has costs. There was no trade-off in generalism from one stage to the next, but worms spent less time growing and developing in stages where they infected more taxonomically diverse hosts. Our results demonstrate that life-cycle complexity favors high generalism and that host use across life stages is determined by both ecological opportunity and life-history trade-offs.

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.

Improving the ability of a BACI design to detect impacts within a kelp-forest community.

Distinguishing between human impacts and natural variation in abundance remains difficult because most species exhibit complex patterns of variation in space and time. When ecological monitoring data are available, a before-after-control-impact (BACI) analysis can control natural spatial and temporal variation to better identify an impact and estimate its magnitude. However, populations with limited distributions and confounding spatial-temporal dynamics can violate core assumptions of BACI-type designs. In this study, we assessed how such properties affect the potential to identify impacts. Specifically, we quantified the conditions under which BACI analyses correctly (or incorrectly) identified simulated anthropogenic impacts in a spatially and temporally replicated data set of fish, macroalgal, and invertebrate species found on nearshore subtidal reefs in southern California, USA. We found BACI failed to assess very localized impacts, and had low power but high precision when assessing region-wide impacts. Power was highest for severe impacts of moderate spatial scale, and impacts were most easily detected in species with stable, widely distributed populations. Serial autocorrelation in the data greatly inflated false impact detection rates, and could be partly controlled for statistically, while spatial synchrony in dynamics had no consistent effect on power or false detection rates. Unfortunately, species that offer high power to detect real impacts were also more likely to detect impacts where none had occurred. However, considering power and false detection rates together can identify promising indicator species, and collectively analyzing data for similar species improved the net ability to assess impacts. These insights set expectations for the sizes and severities of impacts that BACI analyses can detect in real systems, point to the importance of serial autocorrelation (but not of spatial synchrony), and indicate how to choose the species, and groups of species, that can best identify impacts.

At Palmyra Atoll, the fish-community environmental DNA signal changes across habitats but not with tides.

At Palmyra Atoll, the environmental DNA (eDNA) signal on tidal sand flats was associated with fish biomass density and captured 98%-100% of the expected species diversity there. Although eDNA spilled over across habitats, species associated with reef habitat contributed more eDNA to reef sites than to sand-flat sites, and species associated with sand-flat habitat contributed more eDNA to sand-flat sites than to reef sites. Tides did not disrupt the sand-flat habitat signal. At least 25 samples give a coverage >97.5% at this diverse, tropical, marine system.

Looking where it's hard to see: a case study documenting rare Eucyclogobius newberryi presence in a California lagoon.

Environmental DNA (eDNA) analysis is increasingly used for biomonitoring and research of fish populations and communities by environmental resource managers and academic researchers. Although managers are much interested in expanding the use of eDNA as a survey technique, they are sceptical about both its utility (given that information is often limited to presence/absence of a species) and feasibility (given the need for proper laboratory facilities for sample processing). Nonetheless, under the right circumstances, eDNA analysis is cost-effective compared to many traditional aquatic survey methods and does not disturb habitat or harm the animals being surveyed. This article presents a case study in which eDNA analysis was successfully used to document the presence of a rare fish species in a waterway earmarked for restoration. The authors discuss the conditions that allowed this study to occur quickly and smoothly and speculate on how the goals of researchers and managers can be integrated for efficient and informative use of this tool.

Giant kelp, Macrocystis pyrifera, increases faunal diversity through physical engineering.

Foundation species define the ecosystems they live in, but ecologists have often characterized dominant plants as foundational without supporting evidence. Giant kelp has long been considered a marine foundation species due to its complex structure and high productivity; however, there is little quantitative evidence to evaluate this. Here, we apply structural equation modelling to a 15-year time series of reef community data to evaluate how giant kelp affects the reef community. Although species richness was positively associated with giant kelp biomass, most direct paths did not involve giant kelp. Instead, the foundational qualities of giant kelp were driven mostly by indirect effects attributed to its dominant physical structure and associated engineering influence on the ecosystem, rather than by its use as food by invertebrates and fishes. Giant kelp structure has indirect effects because it shades out understorey algae that compete with sessile invertebrates. When released from competition, sessile species in turn increase the diversity of mobile predators. Sea urchin grazing effects could have been misinterpreted as kelp effects, because sea urchins can overgraze giant kelp, understorey algae and sessile invertebrates alike. Our results confirm the high diversity and biomass associated with kelp forests, but highlight how species interactions and habitat attributes can be misconstrued as direct consequences of a foundation species like giant kelp.

Local extinction of the Asian tiger mosquito (Aedes albopictus) following rat eradication on Palmyra Atoll.

The Asian tiger mosquito, Aedes albopictus, appears to have been extirpated from Palmyra Atoll following rat eradication. Anecdotal biting reports, collection records, and regular captures in black-light traps showed the species was present before rat eradication. Since then, there have been no biting reports and no captures over 2 years of extensive trapping (black-light and scent traps). By contrast, the southern house mosquito, Culex quinquefasciatus, was abundant before and after rat eradication. We hypothesize that mammals were a substantial and preferred blood meal for Aedes, whereas Culex feeds mostly on seabirds. Therefore, after rat eradication, humans and seabirds alone could not support positive population growth or maintenance of Aedes This seems to be the first documented accidental secondary extinction of a mosquito. Furthermore, it suggests that preferred host abundance can limit mosquito populations, opening new directions for controlling important disease vectors that depend on introduced species like rats.

Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host.

Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that village, presumably because prawn predation reduced the abundance and average life span of latently infected snails. As expected from a reduction in infected snails, human schistosomiasis prevalence was 18 ± 5% lower and egg burden was 50 ± 8% lower at the prawn-stocking village compared with the control village. In a mathematical model of the system, stocking prawns, coupled with infrequent mass drug treatment, eliminates schistosomiasis from high-transmission sites. We conclude that restoring river prawns could be a novel contribution to controlling, or eliminating, schistosomiasis.

Seroprevalence of Baylisascaris procyonis Infection among Humans, Santa Barbara County, California, USA, 2014-2016.

Baylisascaris procyonis (raccoon roundworm) infection is common in raccoons and can cause devastating pathology in other animals, including humans. Limited information is available on the frequency of asymptomatic human infection. We tested 150 adults from California, USA, for B. procyonis antibodies; 11 were seropositive, suggesting that subclinical infection does occur.

A life cycle database for parasitic acanthocephalans, cestodes, and nematodes.

Parasitologists have worked out many complex life cycles over the last ~150 yr, yet there have been few efforts to synthesize this information to facilitate comparisons among taxa. Most existing host-parasite databases focus on particular host taxa, do not distinguish final from intermediate hosts, and lack parasite life-history information. We summarized the known life cycles of trophically transmitted parasitic acanthocephalans, cestodes, and nematodes. For 973 parasite species, we gathered information from the literature on the hosts infected at each stage of the parasite life cycle (8,510 host-parasite species associations), what parasite stage is in each host, and whether parasites need to infect certain hosts to complete the life cycle. We also collected life-history data for these parasites at each life cycle stage, including 2,313 development time measurements and 7,660 body size measurements. The result is the most comprehensive data summary available for these parasite taxa. In addition to identifying gaps in our knowledge of parasite life cycles, these data can be used to test hypotheses about life cycle evolution, host specificity, parasite life-history strategies, and the roles of parasites in food webs.

Densovirus associated with sea-star wasting disease and mass mortality.

Populations of at least 20 asteroid species on the Northeast Pacific Coast have recently experienced an extensive outbreak of sea-star (asteroid) wasting disease (SSWD). The disease leads to behavioral changes, lesions, loss of turgor, limb autotomy, and death characterized by rapid degradation ("melting"). Here, we present evidence from experimental challenge studies and field observations that link the mass mortalities to a densovirus (Parvoviridae). Virus-sized material (i.e., <0.2 µm) from symptomatic tissues that was inoculated into asymptomatic asteroids consistently resulted in SSWD signs whereas animals receiving heat-killed (i.e., control) virus-sized inoculum remained asymptomatic. Viral metagenomic investigations revealed the sea star-associated densovirus (SSaDV) as the most likely candidate virus associated with tissues from symptomatic asteroids. Quantification of SSaDV during transmission trials indicated that progression of SSWD paralleled increased SSaDV load. In field surveys, SSaDV loads were more abundant in symptomatic than in asymptomatic asteroids. SSaDV could be detected in plankton, sediments and in nonasteroid echinoderms, providing a possible mechanism for viral spread. SSaDV was detected in museum specimens of asteroids from 1942, suggesting that it has been present on the North American Pacific Coast for at least 72 y. SSaDV is therefore the most promising candidate disease agent responsible for asteroid mass mortality.

Revisiting Paine's 1966 Sea Star Removal Experiment, the Most-Cited Empirical Article in the American Naturalist.

"Food Web Complexity and Species Diversity" (Paine 1966) is the most-cited empirical article published in the American Naturalist. In short, Paine removed predatory sea stars (Pisaster ochraceus) from the rocky intertidal and watched the key prey species, mussels (Mytilus californianus), crowd out seven subordinate primary space-holding species. However, because these mussels are a foundational species, they provide three-dimensional habitat for over 300 associated species inhabiting the mussel beds; thus, removing sea stars significantly increases community-wide diversity. In any case, most ecologists cite Paine (1966) to support a statement that predators increase diversity by interfering with competition. Although detractors remained skeptical of top-down effects and keystone concepts, the paradigm that predation increases diversity spread. By 1991, "Food Web Complexity and Species Diversity" was considered a classic ecological paper, and after 50 years it continues to influence ecological theory and conservation biology.

The role of competition--colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence.

Competition - colonization tradeoffs occur in many systems, and theory predicts that they can strongly promote species coexistence. However, there is little empirical evidence that observed competition - colonization tradeoffs are strong enough to maintain diversity in natural systems. This is due in part to a mismatch between theoretical assumptions and biological reality in some systems. We tested whether a competition - colonization tradeoff explains how a diverse trematode guild coexists in California horn snail populations, a system that meets the requisite criteria for the tradeoff to promote coexistence. A field experiment showed that subordinate trematode species tended to have higher colonization rates than dominant species. This tradeoff promoted coexistence in parameterized models but did not fully explain trematode diversity and abundance, suggesting a role of additional diversity maintenance mechanisms. Spatial heterogeneity is an alternative way to promote coexistence if it isolates competing species. We used scale transition theory to expand the competition - colonization tradeoff model to include spatial variation. The parameterized model showed that spatial variation in trematode prevalence did not isolate most species sufficiently to explain the overall high diversity, but could benefit some rare species. Together, the results suggest that several mechanisms combine to maintain diversity, even when a competition - colonization tradeoff occurs.

The role of competition - colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence.

Competition - colonization tradeoffs occur in many systems, and theory predicts that they can strongly promote species coexistence. However, there is little empirical evidence that observed competition- colonization tradeoffs are strong enough to maintain diversity in natural systems. This is due in part to a mismatch between theoretical assumptions and biological reality in some systems. We tested whether a competition - colonization tradeoff explains how a diverse trematode guild coexists in California horn snail populations, a system that meets the requisite criteria for the tradeoff to promote coexistence. A field experiment showed that subordinate trematode species tended to have higher colonization rates than dominant species. This tradeoff promoted coexistence in parameterized models but did not fully explain trematode diversity and abundance, suggesting a role of additional diversity maintenance mechanisms. Spatial heterogeneity is an alternative way to promote coexistence if it isolates competing species. We used scale transition theory to expand the competition - colonization tradeoff model to include spatial variation. The parameterized model showed that spatial variation in trematode prevalence did not isolate most species sufficiently to explain the overall high diversity, but could benefit some rare species. Together, the results suggest that several mechanisms combine to maintain diversity, even when a competition - colonization tradeoff occurs.

Parasites affect food web structure primarily through increased diversity and complexity.

Comparative research on food web structure has revealed generalities in trophic organization, produced simple models, and allowed assessment of robustness to species loss. These studies have mostly focused on free-living species. Recent research has suggested that inclusion of parasites alters structure. We assess whether such changes in network structure result from unique roles and traits of parasites or from changes to diversity and complexity. We analyzed seven highly resolved food webs that include metazoan parasite data. Our analyses show that adding parasites usually increases link density and connectance (simple measures of complexity), particularly when including concomitant links (links from predators to parasites of their prey). However, we clarify prior claims that parasites "dominate" food web links. Although parasites can be involved in a majority of links, in most cases classic predation links outnumber classic parasitism links. Regarding network structure, observed changes in degree distributions, 14 commonly studied metrics, and link probabilities are consistent with scale-dependent changes in structure associated with changes in diversity and complexity. Parasite and free-living species thus have similar effects on these aspects of structure. However, two changes point to unique roles of parasites. First, adding parasites and concomitant links strongly alters the frequency of most motifs of interactions among three taxa, reflecting parasites' roles as resources for predators of their hosts, driven by trophic intimacy with their hosts. Second, compared to free-living consumers, many parasites' feeding niches appear broader and less contiguous, which may reflect complex life cycles and small body sizes. This study provides new insights about generic versus unique impacts of parasites on food web structure, extends the generality of food web theory, gives a more rigorous framework for assessing the impact of any species on trophic organization, identifies limitations of current food web models, and provides direction for future structural and dynamical models.