Sergio A. Navarrete

The Keystone Species Concept: Variation in Interaction Strength in a Rocky Intertidal Habitat

The usefulness and generality of the keystone species concept has recently been questioned. We investigated variation in interaction strength between the original keystone predator, the seastar Pisaster ochraceus, and its primary prey, mussels (Mytilus californianus and M. trossulus). The study was prompted by differences in community structure at two low zone sites along the central Oregon coast, Boiler Bay (BB) and Strawberry Hill (SH). Predators, especially seastars, were larger and more abundant at SH than at BB. Further, sessile animals were more abundant and macrophytes were less abundant at SH. Predators were more abundant at wave—exposed sites at both sites, and at SH, sessile invertebrates were more abundant at the wave—exposed location and sand cover was high at the wave—protected location. To test the hypothesis that variation in predation strength explained some of these differences, we examined the seastar—mussel interaction at locations with high and low wave exposure at both sites. Predation intensity was quantified by determining the survival of mussels in clumps (50 mussels per clump, shell length 4—7 cm) transplanted to large plots (18—163 m2) with or without seastars in the low intertidal zone. Predation effects were quantified by determining prey recolonization rates in marked quadrats in the same large plots. Spatial variation in interaction strength was quantified by examining predation at scales of metres (among transplants within plots), 10s of metres (between replicate plots within each exposure at each site), 100s of metres (between wave exposures within locations), and 10 000s of metres (between sites). Temporal variation was evaluated by performing the experiments in 1990 and 1991. The relation between prey (mussel) recruitment and growth to differences in community structure was evaluated by quantifying recruitment density in plastic mesh balls (collectors) and growth of individually marked transplanted mussels, respectively, at each site ° exposure ° tide level combination each month for 4 yr. Predation intensity varied greatly at all spatial scales. At the two largest spatial scales (10s of kilometres, 100s of metres), differences in both survival of transplanted mussels and prey recolonization depended on variation in seastar abundance with site, wave exposure, prey recruitment and growth, and at SH protected, the extent of sand burial. Variation at the two smallest scales (metres, 10s of metres) was high when seastars were scarce and low when seastars were abundant. Transplanted mussels suffered 100% mortality in 2 wk at wave—exposed SH, but took >52 wk at wave—protected BB. Seastar effects on prey recolonization were detected only at the SH wave—exposed site. Here, where prey recruitment and growth were unusually high, the mussel M. trossulus invaded and dominated space within 9 mo. After 14 mo, whelks, which increased in both size and abundance in the absence of Pisaster, arrested this increase in mussel abundance. Similar changes did not occur at other site ° exposure combinations, evidently because prey recruitment was low and possibly also due to whelk predation on juveniles. Longer term results indicate that, as in Washington state, seastars prevent large adult M. californianus from invading lower intertidal regions, but only at wave—exposed, not wave—protected sites. Thus, three distinct predation regimes were observed: (1) strong keystone predation by seastars at wave—exposed headlands; (2) less—strong diffuse predation by seastars, whelks, and possibly other predators at a wave—protected cove, and (3) weak predation at a wave—protected site buried regularly by sand. Comparable experimental results at four wave—exposed headlands (our two in Oregon and two others in Washington), and similarities between these and communities on other West Coast headlands suggest keystone predation occurs broadly in this system. Results in wave—protected habitats, however, suggest it is not universal. In Oregon, keystone predation was evidently contingent on conditions of high prey production (i.e., recruitment and growth), while diffuse predation occurred when prey production was low, and weak predation occurred when environmental stress was high. Combining our results with examples from other marine and non—marine habitats suggests a need to consider a broader range of models than just keystone predation. The predictive and explanatory value of an expanded set of models depends on identifying factors distinguishing them. Although evidence is limited, a survey of 17 examples suggests (1) keystone predation is evidently not distinguished from diffuse predation by any of 11 previously proposed differences, but (2) may be distinguished by rates of prey production. Further, (3) differential predation on competitively dominant prey does not distinguish keystone from nonkeystone systems, since this interaction occurs in both types of community. Instead, differential predation on dominant prey evidently distinguishes strong—from weak—predation communities. While the keystone predation concept has been and will continue to be useful, a broadened focus on testing and developing more general models of community regulation is needed.

Integrating abundance and functional traits reveals new global hotspots of fish diversity

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao’s Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites (‘community evenness’), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

Keystone Predation and Interaction Strength: Interactive Effects of Predators on Their Main Prey

The application of basic ecological concepts to fields of conservation biology and applied environmental sciences is a healthy sign, but before these concepts are widely used, ecology must provide operational definitions and quantifiable methods. Keystone species and interaction strength are concepts with deep practical and theoretical implications. We studied the strength of predation on mussels (Mytilus trossulus) by the keystone seastar Pisaster ochraceus and the whelks Nucella emarginata and N. canaliculata under different environmental conditions in the Oregon intertidal zone. We attempted to determine: (1) the sensitivity of keystone predation to the presence of other predators in the system; (2) the role of other predators in the presence and absence of a keystone species; and (3) the per capita and population—level variability in interaction strengths of strong (keystone) vs. weak interactors. Predation intensity on mussels was measured by recording the survival of mussels transplanted to areas from which seastars, whelks, or both, had been either manually removed or left undisturbed at natural densities. Whelk experimental units were nested within those for the seastar treatment to account for the much larger body size and greater mobility of seastars. Each combination of seastar and whelk treatment was replicated four times in both wave—exposed and wave—protected habitats of two sites that differed in predator densities, primary productivity, and recruitment and growth rates of prey species. Predation intensity by the keystone predator was strong under all site

More than a meal… integrating non‐feeding interactions into food webs

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SCALING POPULATION DENSITY TO BODY SIZE IN ROCKY INTERTIDAL COMMUNITIES

wave exposure combinations, and was unaffected by the presence of whelks. Whelks, in contrast, had ecologically important effects on mussel survival in the absence, but not in the presence, of the keystone predator. Population (total) interaction strength between seastars and mussels was 2—10 times stronger than that between whelks and mussels across sites and wave exposures. Per capita interaction strength of seastars was two to three orders of magnitude larger than that of whelks. However, per capita effects of seastars were more variable between sites and wave exposures, probably because simple density values grossly underestimate the ability of mobile predators to localize prey. Such interactive effects and variability in interaction strengths between keystone and weak predators may characterize all keystone predator—dominated systems, but data currently are insufficient to test this proposition. Negative effects of seastars on whelk density were observed <4 mo following initiation of Pisaster removals. Seastars also had a negative effect on whelk sizes, which took longer to appear, after 6 mo of continuous Pisaster removal. Negative effects of seastars on whelks appeared to be stronger in places with higher densities of predators, partially explaining the reduced predation intensity of whelks observed in the presence of seastars. Our results support the idea that in keystone—dominated systems, species other than the keystone species have only minor, if any, effects on the rest of the community, and thus might be cited by some as redundant species. However, our results also indicate that, after the loss of a keystone species, previously redundant species can partially compensate for the reduced predation and adopt a major role in the altered system. Such responses are potentially an important force in stabilizing communities. Further, such possible compensatory capabilities of alternative consumers suggests that, at least for predators, the term redundant species conveys an inaccurate image of the potential importance of weak interactors and should be abandoned.

Diversity, dynamics and biogeography of Chilean benthic nearshore ecosystems: an overview and guidelines for conservation

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.

Variable Predation: Effects of Whelks on a Mid-Intertidal Successional Community

Interspecific comparisons of animal population density to body size has been the subject of active research in the last decade, especially for terrestrial animals when considering particular taxa or taxonomic assemblages. Studies of rocky intertidal communities showed that animal population density scales with body size to the -0.77 power. This relation held within local communities representing a broad array of animal taxa and was not affected by a dramatic alteration in the network of between-species interactions, as revealed by two long-term human exclusion experiments.

Crisis on coral reefs linked to climate change

A pesar de que Chile ha sido un pais pionero en estudios del efecto del impacto humano sobre la estructura comunitaria en ambientes marinos, y a pesar de la enorme importancia economica y social que el ambiente marino tiene para el pais, el desarrollo de programas de conservacion marina y de bases cientificas para la sustentabilidad no se han generado a la misma tasa a la que han explotado los recursos y se ha utilizado el ambiente costero para diversos fines. Aunque nosotros pensamos que el establecimiento de planes de conservacion a lo largo de la costa de Chile debe basarse en varios factores, los principios cientificos, biologicos y ecologicos deben guiar muchos de estos esfuerzos, y en este trabajo nosotros intentamos presentar una vision general del estado actual del conocimiento sobre la ecologia y la biogegrafia del sistema costero en Chile. En base a la informacion mas relevante existente, nuestros objetivos son: 1) identificar las caracteristicas biogeograficas y ecologicas del ecosistema costero y tambien vacios en informacion, 2) identificar las actividades humanas mas daninas que tengan impacto en la estructura y dinamica de estos sistemas, y 3) sugerir el uso de posibles indicadores para determinar la situacion de diferentes areas de la costa de Chile, y las necesidades de conservacion. Esta revision muestra, por un lado, areas geograficas con informacion critica deficitaria para planes futuros de manejo y conservacion marina , y por el otro lado, la disponibilidad de informacion de alta calidad para otras zonas geograficas del pais. Respecto de la informacion existente sobre taxonomia y patrones de distribucion de especies a gran escala, existen importantes vacios de informacion; no se esperan en el futuro grandes cambios en el numero total de especies. Existen pocos estudios sobre patrones de distribucion de especies a gran escala, y mas informacion es necesaria para identificar areas de alta diversidad de especies, especialmente para algunos taxa, como tambien para identificar areas que posean caracteristicas unicas en relacion a especies (endemicas, especies claves) y a procesos ecosistemicos (disturbios, surgencias). Para la mayoria de los invertebrados y macroalgas, las areas de alta diversidad de especies se encuentran en el sur de Chile. Nuevos estudios dirigidos a entender los factores que podrian generar patrones a macroescala son necesarios, como tambien informacion sobre oceanografia costera y disponibilidad de larvas. Esta informacion es clave para el diseno de una futura red de parques marinos. Por otro lado, la informacion disponible sobre estructuras comunitarias y funcionamiento ecosistemico, especialmente sobre el efecto del impacto humano, provienen de pocas regiones geograficas. Mas informacion sobre otras zonas geograficas es requerida, particularmente si se consideran las diferencias notables en temperatura, patrones de circulacion, heterogeneidad del habitat, y composicion de especies, como tambien el efecto de surgencia y de El Nino a lo largo de los mas de 4.000 km de costa de Chile. Finalmente, listamos las que consideramos son las actividades humanas mas daninas para el ambiente marino, e integramos esta informacion para sugerir posibles indicadores ambientales y necesidades basicas y sugerencias para conservacion marina in Chile

Scaling of Food-Web Properties with Diversity and Complexity Across Ecosystems

In most habitats and ecosystems, predation varies significantly over space and over time. While several studies have demonstrated the effects of varying predation intensities, the effects of varying frequencies of predation have not been addressed ex- plicitly. Here, I studied the impact of variable predation by whelks on a mid-intertidal successional community at a wave-exposed environment on the coast of Oregon. Densities of whelks were monitored in fixed-position quadrats for 34 mo, permitting an estimation of the natural spatial and temporal variation in predation by whelks. Two simultaneous cage experiments were then conducted for a period of 25 mo. One experiment evaluated the effect of prolonged exclusion of invertebrate predators on the sessile community. The other experiment evaluated the effects of the intensity and the temporal frequency of pre- dation by whelks by manipulating both the density and presence of whelks inside cages. Three density levels were combined with three temporal patterns of predation (constant predation, medium and low frequency) in an orthogonal design to create nine different predation regimes. The replicated design allowed me to separate the effects of these two components of predation. The densities of the two whelk species present in the study site, Nucella canaliculata and N. emarginata, were highly correlated over time and varied greatly within and among years. Some areas of the site had whelks present most of the time (high frequency),,.while other areas were rarely visited. The frequency at which whelks were observed in a given area was uncorrelated with the yearly mean density, which contributed to the within-habitat variability in predation regimes by whelks. A suite of direct and indirect effects were observed following the permanent exclusion of invertebrate predators, notably, a rapid increase in the cover of the bay mussel Mytilus trossulus and a slow and small increase in the cover of gooseneck barnacles and the California mussel Mytilus californianus. Tem- porally variable predation (medium and low frequencies) produced community compositions different from those observed under a constant predation regime or predator exclusions. In general, individual species responses to variable predation could not be predicted from knowledge of the overall effect of predators obtained in the permanent exclusion experiment, nor from the results observed under different intensities and constant predation. Similarly, the actual number of predation days, estimated from the density and number of days whelks were in the cages, was not correlated with the mean cover of species. These results support the hypothesis that temporal frequency is an important component of predation with dis- tinctive effects on intertidal prey communities. Both the ability of some prey to escape predators by reaching a large size and the temporal pattern of prey recruitment seemed important in determining the effect of variable predation on individual prey, but mechanistic understanding of the responses was complicated by the existence of many indirect effects. While temporally variable predation did not significantly increase spatial variability in prey abundance, constant predation regimes tended to reduce this variability over the course of succession. Temporal variability in predation by whelks can have distinctive effects on prey, create distinctive community compositions, and affect successional paths in this intertidal com- munity. Temporal variability in predation is probably an important, yet poorly understood cause of spatial heterogeneity in most ecosystems.

Resource partitioning between intertidal predatory crabs: interference and refuge utilization

Since 1982, coral reefs worldwide have been subjected to an increased frequency of the phenomenon known as coral bleaching. Bleaching involves the dramatic loss of pigmented, single-celled endosymbiotic algae that live within the gastrodermal cells of a coral host that depends on this relationship for survival. Prior to the 1980s, and as early as the 1920s when coral reef research intensified, localized bleaching events were reported and attributed to factors such as extremely low tides, hurricane damage, torrential rainstorms, freshwater runoff near reefs, or toxic algal blooms [Glynn, 1993]. However, these early occurrences have recently been overshadowed by geographically larger and more frequent bleaching events whose impact has expanded to regional and global proportions.