Herbivorous sea urchins (Echinometra mathaei) support resilience on overfished and sedimented tropical reefs.

Human impacts are dramatically changing ecological communities, motivating research on resilience. Tropical reefs are increasingly undergoing transitions to short algal turf, a successional community that mediates either recovery to coral by allowing recruitment or transitions to longer turf/macroalgae. Intense herbivory limits turf height; subsequently, overfishing erodes resilience of the desirable coral-dominated reef state. Increased sedimentation also erodes resilience through smothering and herbivory suppression. In spite of this critical role, most herbivory studies on tropical reefs focus on fishes, and the contribution of urchins remains under-studied. To test how different herbivory and sedimentation scenarios impact turf resilience, we experimentally simulated, in situ, four future overfishing scenarios derived from patterns of fish and urchin loss in other reef systems and two future sedimentation regimes. We found urchins were critical to short turf resilience, maintaining this state even with reduced fish herbivory and increased sediment. Further, urchins cleared sediment, facilitating fish herbivory. This study articulates the likelihood of increased reliance on urchins on impacted reefs in the Anthropocene.

A persistent green macroalgal mat shifts ecological functioning and composition of associated species on an Eastern Tropical Pacific coral reef.

Global evidence of phase shifts to alternate community types is of particular concern because these new communities can provide fundamentally different and often novel ecosystem functions and services compared to the original community. Shifts of a diverse range of marine communities to dominance by green macroalgal mats have occurred worldwide, making it critical to understand their emerging functions and roles. We observed a green algal mat on two reefs in the Eastern Tropical Pacific, with one persisting for >10 years on a reef with stable herbivore populations and no known sources of anthropogenic nutrients. These mats supported a more speciose macroalgal community with fewer taxa present in the adjacent coral community and facilitated growth of an associated understory macroalgal species by reducing herbivory pressure and possibly enhancing nutrient supplies within the mat community state. These results demonstrate a weakening in the processes controlling reef community structure as a result of the shift in composition associated with the macroalgal mat, creating a positive feedback supporting mat persistence. These novel ecosystem functions generated by this alternate community state illustrate the importance of further research on community shifts, which will become increasingly common in the Anthropocene.

Ontogenetic Variation in Blade Toughness May Contribute to the Spread of Turbinaria ornata Across the South Pacific.

Coral reefs are shifting from coral to algal-dominated ecosystems worldwide. Recently, Turbinaria ornata, a marine alga native to coral reefs of the South Pacific, has spread in both range and habitat usage. Given dense stands of T. ornata can function as an alternative stable state on coral reefs, it is imperative to understand the factors that underlie its success. We tested the hypothesis that T. ornata demonstrates ontogenetic variation in allocation to anti-herbivore defense, specifically that blade toughness varied nonlinearly with thallus size. We quantified the relationship between T. ornata blade toughness and thallus size for individual thalli within algal stands (N = 345) on seven fringing reefs along the north shore of Moorea, French Polynesia. We found that blade toughness was greatest at intermediate sizes that typically form canopies, with overall reduced toughness in both smaller individuals that refuge within the understory and older reproductive individuals that ultimately detach and form floating rafts. We posit this variation in blade toughness reduces herbivory on the thalli that are most exposed to herbivores and may facilitate reproduction in dispersing stages, both of which may aid the proliferation of T. ornata.

Flip it and reverse it: Reasonable changes in designated controls can flip synergisms to antagonisms.

Ecological systems are subjected to multiple stressors that can interact in complex ways resulting in "ecological surprises". We examine the pivotal role of 'control' assignment in the categorization of stressors into five classes: additive, +synergistic, -synergistic, +antagonistic, and -antagonistic. We demonstrate if an alternate treatment can reasonably be considered the experimental control, nonlinear interaction classifications change, both in sign (+/-) and in direction (synergistic/antagonistic). Further, switching of interaction classifications is not predictable as changing control can result in multiple possible alternate nonlinear classifications. To explore the magnitude of this problem, we evaluate publications gathered for a recent meta-analysis to 1) explore rationales for choice of controls and 2) quantify how frequently it is reasonable to reassign the control. We found controls were designated with a variety of implicit and explicit justifications, with two overall rationales: 1) controls based on 'natural' conditions (historic, current, or future); 2) controls based on direction of impact, such that stressors always have negative impacts. We reasoned that control re-assignment was justified if an alternate treatment met one of these rationales. Of the 844 interactions classified in the meta-analysis, we determined >95% could be reassigned. Based on these findings, we recommend a new approach to meta-analyses, where the 'control' is strictly and consistently defined by the authors of the meta-analysis. These controls should be based on their broader question, rather than following the common practice of defaulting to controls assigned by the authors of each study, as we found these rationales vary broadly based on the specific questions of each study. Consistent control designation within the ecological or toxicological framework of each meta-analysis may provide deeper and more consistent insight into the nature of interactive effects between multiple stressors. Gaining this insight is crucial because stressor interactions are certain to increase in the Anthropocene.

Storms may disrupt top-down control of algal turf on fringing reefs.

Storms strongly affect coral reefs; one unstudied but potentially important outcome may be a decrease in herbivory, presumably through changes to freshwater, sediment and nutrient influx. Algal turfs are sensitive early indicators of reef condition, and experimental evidence demonstrates low sediment loads and strong herbivory maintain short, healthy turf. While unknown, storms likely disrupt these controlling forces. We have observed storms that generate frequent, visible sediment plumes in Moorea, French Polynesia. To evaluate the effects of storms on herbivory, we conducted a set of field experiments manipulating herbivore access to naturally occurring turf under three rainfall regimes: no rain, light rain, and heavy rain that generated a plume event. We found strong effects of herbivores except following the storm, indicating disruption of typically strong top-down control by herbivores on algal turfs. Further research into the underlying mechanisms is critical as storm intensities and watershed development increase in many tropical regions.

Extreme rainfall events pulse substantial nutrients and sediments from terrestrial to nearshore coastal communities: a case study from French Polynesia.

Rainfall mobilizes and transports anthropogenic sources of sediments and nutrients from terrestrial to coastal marine ecosystems, and episodic but extreme rainfall may drive high fluxes to marine communities. Between January 13th and January 22nd, 2017, the South Pacific Island of Moorea, French Polynesia experienced an extreme rainfall event. ~57 cm of rain was delivered over a 10-day storm. We quantified pulsed sediments and nutrients transported to nearshore reefs. We determined the spatial and temporal extent of the sediment pulse with estimates of water transparency. We quantified pulsed nutrients at multiple spatial and temporal scales. To determine if terrestrial nutrients were incorporated into the benthic community, we collected macroalgae over 10 days following the storm and measured tissue nutrient concentrations and δN15. Pulsed sediments impacted water clarity for 6 days following the storm, with greatest impacts closest to the river mouth. Nitrite +nitrate concentrations were >100 times the average while phosphate was >25 times average. Macroalgal tissue nutrients were elevated, and δN15 implicates sewage as the source, demonstrating transported nutrients were transferred to producer communities. Future climate change predictions suggest extreme rainfall will become more common in this system, necessitating research on these pulses and their ramifications on marine communities.

TESTING THE CONCEPTUAL AND OPERATIONAL UNDERPINNINGS OF HERBIVORY ASSAYS: DOES VARIATION IN PREDICTABILITY OF RESOURCES, ASSAY DESIGN, AND DEPLOYMENT METHOD AFFECT OUTCOMES?

Herbivory assays are a valuable tool used by ecologists to understand many of the patterns and processes affecting herbivory, a widely recognized driving force in marine communities. However, methods vary substantially among studies in both design and operation, and the effect of these differences has yet to be evaluated. We assessed the effects of several key components of assay design on estimates of herbivory to offer four recommendations. First, we found assays out-planted on sequential days in both predictable and random locations within a 60m2 site experienced temporal increases in herbivory by an increasingly diverse assemblage of fishes. Thus, we strongly advise against placing herbivory assays in the same site over a series of days. Second, we found while the amount of biomass consumed in assays was density dependent, the percent loss was not. Thus, we recommend researchers report percent consumption because this metric is robust to differences in biomass offered and will facilitate comparisons across studies. Third, we found associational effects, where proximity of species of differing palatabilities impacted estimates of herbivory rate on one or both species, but these impacts were not consistent across species or sites. Thus, we recommend the effect of association be directly tested for multi specie herbivory assays. Fourth, we found no effect of attachment method on estimates of herbivory rate and recommend researchers continue to use the attachment method in which they are most confident. We hope our experimental results prove useful in the future when designing, conducting, and interpreting herbivory assays.

Hermaphrodites and parasitism: size-specific female reproduction drives infection by an ephemeral parasitic castrator.

Sex can influence patterns of parasitism because males and females can differ in encounter with, and susceptibility to, parasites. We investigate an isopod parasite (Hemioniscus balani) that consumes ovarian fluid, blocking female function of its barnacle host, a simultaneous hermaphrodite. As a hermaphrodite, sex is fluid, and individuals may allocate energy differentially to male versus female reproduction. We predicted the relationship between barnacle size and female reproductive function influences the distribution of parasites within barnacle populations. We surveyed 12 populations spanning ~400 km of coastline of southern California and found intermediate-sized barnacles where most likely to be actively functioning as females. While it is unclear why larger individuals are less likely to be actively reproducing as females, we suggest this reduced likelihood is driven by increased investment in male reproductive effort at larger sizes. The female function-size relationship was mirrored by the relationship between size and parasitism. We suggest parasitism by Hemioniscus balani imposes a cost to female function, reinforcing the lack of investment in female function by the largest individuals. Within the subset of suitable (=female) hosts, infection probability increased with size. Hence, the distribution of female function, combined with selection for larger hosts, primarily dictated patterns of infection.

Parasite and host biomass and reproductive output in barnacle populations in the rocky intertidal zone.

The rocky intertidal zone has a long history of ecological study with barnacles frequently serving as a model system to explore foundational theories. Parasites are often ignored in community ecology studies, and this particularly holds for true for the rocky intertidal zone. We explore the role of the isopod parasite, Hemioniscus balani, on its host, the acorn barnacle, Chthamalus fissus. We use the currencies of biomass and reproduction measured at the individual level, then applied to the population level, to evaluate the importance of this parasite to barnacle populations. We found H. balani can comprise substantial biomass in 'apparent' barnacle populations, sometimes even equaling barnacle biomass. Additionally, parasite reproduction sometimes matched barnacle reproduction. Thus, parasites divert substantial energy flow from the barnacle population and to near-shore communities in the form of parasite larvae. Parasites appeared to decrease barnacle reproduction per area. Potentially, this parasite may control barnacle populations, depending on the extent to which heavily infected barnacle populations contribute to barnacle populations at larger scales. These findings regarding the importance of a particular parasite for host population dynamics in this well studied ecosystem call for the integration of disease dynamics into community ecological studies of the rocky intertidal zone.

Epibionts on Turbinaria ornata, a secondary foundational macroalga on coral reefs, provide diverse trophic support to fishes.

Worldwide, many coral reef ecosystems have shifted from coral to algal dominance, yet the ecological function of these emergent communities remains relatively unknown. Turbinaria ornata, a macroalga with a rapidly expanding range in the South Pacific, forms dense stands on hard substrate, likely providing ecological services unique from corals. While generally unpalatable, T. ornata can function as a secondary foundation species and hosts an epibiont community that may provide overlooked trophic resources in phase shifted reef ecosystems. Results from video recorded field experiments designed to quantify consumer pressure on T. ornata epibionts showed that both consumer pressure and epibiont cover increased with thallus size. Additionally, most fish species, including herbivores, omnivores, and detritivores, exhibited higher bite rates on thalli with epibionts compared to thali with epibionts experimentally removed. Juvenile parrotfishes were responsible for 50% of total bites recorded and also had the highest bite rates. Results indicate that epibionts, particularly on large T. ornata, are a food resource for a diversity of fishes, representing a previously undescribed function of this macroalga in coral reef ecosystems. Exploring the functions of macroalgal dominated reef communities will be increasingly important as reefs continue to phase shift toward macroalgal dominance in the Anthropocene.

Empirical data demonstrates risk-tradeoffs between landscapes for herbivorous fish may promote reef resilience.

Herbivores balance resource requirements with predation risk, which can differ among landscapes; hence, landscape can shape these trade-offs, influencing herbivore distribution and behavior. While this paradigm has been well established on coral-dominated reefs, tropical reefs worldwide are shifting to algal dominance. If herbivores avoid algae due to higher risk and forage in coral, these algal states may be stabilized. However, if herbivores forage more in resource-rich algal states, this may promote coral recovery. We assessed the distribution and behavior of herbivorous fishes in Moorea, French Polynesia in coral and algal turf-dominated fringing reef sites. Acanthuridae were more abundant in coral states and Labridae, tribe Scarinae, in algal turf states, though total fish abundances were equivalent in the two states. Fish in both families spent more time feeding in algal states and hiding/swimming in coral states. Thus, behavior reflects the trade-off between resource acquisition and refuge in these two landscapes and may promote recovery to coral.

Predation on transmission stages reduces parasitism: sea anemones consume transmission stages of a barnacle parasite.

While parasites serve as prey, it is unclear how the spatial distribution of parasite predators provides transmission control and influences patterns of parasitism. Because many of its organisms are sessile, the rocky intertidal zone is a valuable but little used system to understand spatial patterns of parasitism and elucidate the underlying mechanisms driving these patterns. Sea anemones and barnacles are important space competitors in the rocky intertidal zone along the Pacific coast of North America. Anemones are voracious, indiscriminate predators; thus, they may intercept infectious stages of parasites before they reach a host. We investigate whether a sea anemone protects an associated barnacle from parasitism by Hemioniscus balani, an isopod parasitic castrator. At Coal Oil Point, Santa Barbara, California USA, 29% of barnacles were within 1 cm from an anemone at the surveyed tidal height. Barnacles associated with anemones had reduced parasite prevalence and higher reproductive productivity than those remote from sea anemones. In the laboratory, anemones readily consumed the transmission stage of the parasite. Hence, anemone consumption of parasite transmission stages may provide a mechanism by which community context regulates parasite prevalence at a local scale. Our results suggest predation may be an important process providing parasite transmission control.

Two's a crowd? Crowding effect in a parasitic castrator drives differences in reproductive resource allocation in single vs double infections.

The 'crowding effect' is a result of competition by parasites within a host for finite resources. Typically, the severity of this effect increases with increasing numbers of parasites within a host and manifests in reduced body size and thus fitness. Evidence for the crowding effect is mixed - while some have found negative effects, others have found a positive effect of increased parasite load on parasite fitness. Parasites are consumers with diverse trophic strategies reflected in their life history traits. These distinctions are useful to predict the effects of crowding. We studied a parasitic castrator, a parasite that usurps host reproductive energy and renders the host sterile. Parasitic castrators typically occur as single infections within hosts. With multiple parasitic castrators, we expect strong competition and evidence of crowding. We directly assess the effect of crowding on reproductive success in a barnacle population infected by a unique parasitic castrator, Hemioniscus balani, an isopod parasite that infects and blocks reproduction of barnacles. We find (1) strong evidence of crowding in double infections, (2) increased frequency of double infections in larger barnacle hosts with more resources and (3) perfect compensation in egg production, supporting strong space limitation. Our results document that the effects of crowding are particularly severe for this parasitic castrator, and may be applicable to other castrators that are also resource or space limited.

Why species matter: an experimental assessment of assumptions and predictive ability of two functional-group models.

Community ecologists use functional groups based on the rarely tested assumption that within-group responses to ecological processes are similar and thus members are functionally equivalent. However, recent research suggests that functional equivalency may break down with human impacts. We tested the equivalency assumption and model predictions of responses to simulated human alterations in nutrients and large herbivores for two models of coral reef algae, the Relative Dominance Model (RDM) and the Functional Group Model (FGM). Results of both mesocosm and field experiments using assembled communities were compared to model predictions, and within- and between-group variability were assessed. Both models' predictions of group response to herbivory matched experimental outcomes, but only the RDM predicted response to nutrients. However, within-group variability was dramatic, because the RDM grouped species with opposite responses to herbivory and the FGM grouped species with unique responses to nutrients. These heterogeneous responses resulted in loss of information and masked strong interactions between herbivory and nutrients that were not included in the models. As humans continue to impact major ecological processes in ecosystems globally, we postulate that functional-group models may need to be reformulated to account for shifting baselines.

Cnidocyte discharge is regulated by light and opsin-mediated phototransduction.

BACKGROUND: Cnidocytes, the eponymous cell type of the Cnidaria, facilitate both sensory and secretory functions and are among the most complex animal cell types known. In addition to their structural complexity, cnidocytes display complex sensory attributes, integrating both chemical and mechanical cues from the environment into their discharge behavior. Despite more than a century of work aimed at understanding the sensory biology of cnidocytes, the specific sensory receptor genes that regulate their function remain unknown. RESULTS: Here we report that light also regulates cnidocyte function. We show that non-cnidocyte neurons located in battery complexes of the freshwater polyp Hydra magnipapillata specifically express opsin, cyclic nucleotide gated (CNG) ion channel and arrestin, which are all known components of bilaterian phototransduction cascades. We infer from behavioral trials that different light intensities elicit significant effects on cnidocyte discharge propensity. Harpoon-like stenotele cnidocytes show a pronounced diminution of discharge behavior under bright light conditions as compared to dim light. Further, we show that suppression of firing by bright light is ablated by cis-diltiazem, a specific inhibitor of CNG ion channels. CONCLUSIONS: Our results implicate an ancient opsin-mediated phototransduction pathway and a previously unknown layer of sensory complexity in the control of cnidocyte discharge. These findings also suggest a molecular mechanism for the regulation of other cnidarian behaviors that involve both photosensitivity and cnidocyte function, including diurnal feeding repertoires and/or substrate-based locomotion. More broadly, our findings highlight one novel, non-visual function for opsin-mediated phototransduction in a cnidarian, the origins of which might have preceded the evolution of cnidarian eyes.

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway.

The evolutionary histories of complex traits are complicated because such traits are comprised of multiple integrated and interacting components, which may have different individual histories. Phylogenetic studies of complex trait evolution often do not take this into account, instead focusing only on the history of whole, integrated traits; for example, mapping eyes as simply present or absent through history. Using the biochemistry of animal vision as a model, we demonstrate how investigating the individual components of complex systems can aid in elucidating both the origins and diversification of such systems. Opsin-based phototransduction underlies all visual phenotypes in animals, using complex protein cascades that translate light information into changes in cyclic nucleotide gated (CNG) or canonical transient receptor potential (TRPC) ion-channel activity. Here we show that CNG ion channels play a role in cnidarian phototransduction. Transcripts of a CNG ion channel co-localize with opsin in specific cell types of the eyeless cnidarian Hydra magnipapillata. Further, the CNG inhibitor cis-diltiazem ablates a stereotypical photoresponse in the hydra. Our findings in the Cnidaria, the only non-bilaterian lineage to possess functional opsins, allow us to trace the history of CNG-based photosensitivity to the very origin of animal phototransduction. Our general analytical approach, based on explicit phylogenetic analysis of individual components, contrasts the deep evolutionary history of CNG-based phototransduction, today used in vertebrate vision, with the more recent assembly of TRPC-based systems that are common to protostome (e.g. fly and mollusc) vision.