A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Predator type influences the frequency of functional responses to prey in marine habitats.

The functional response of a consumer to a gradient of resource density is a widespread and consistent framework used to quantify the importance of consumption to population dynamics and stability. Within benthic marine ecosystems, both crustaceans and fishes can provide strong top-down pressure on prey populations. Taxon-specific differences in biomechanics or habitat use, among other factors, may lead to variable functional response forms or parameter values (attack rate, handling time). Based on a review of 189 individual functional response fits, we find that these predator guilds differ in their frequency distribution of functional response types, with crustaceans exhibiting nearly double the proportion of sigmoidal, density-dependent functional responses (Holling type III) as predatory fishes. The implications of this finding for prey population stability are significant because type III responses allow prey persistence while type II responses are de-stabilizing and can lead to extinction. Comparing per capita predation rates across diverse taxa can provide integrative insights into predatory effects and the ability of predation to drive community structure.

Experiments reveal limited top-down control of key herbivores in southern California kelp forests.

Predator responses to gradients in prey density have important implications for population regulation and are a potential structuring force for subtidal marine communities, particularly on rocky reefs where herbivorous sea urchins can drive community state shifts. On rocky reefs in southern California where predatory sea otters have been extirpated, top-down control of sea urchins by alternative predators has been hypothesized but rarely tested experimentally. In laboratory feeding assays, predatory spiny lobsters (Panulirus interruptus) demonstrated a saturating functional response to urchin prey, whereby urchin proportional mortality was inversely density-dependent. In field experiments on rocky reefs near San Diego, California, predators (primarily the labrid fish California sheephead, Semicossyphus pulcher) inflicted highly variable mortality on purple urchin (Strongylocentrotus purpuratus) prey across all density levels. However, at low to moderate densities commonly observed within kelp forests, purple urchin mortality increased to a peak at a density of ~11 urchins/m2 . Above that level, at densities typical of urchin barrens, purple urchin mortality was density-independent. When larger red urchins (Mesocentrotus franciscanus) were offered to predators simultaneously with purple urchins, mortality was density-independent. Underwater videography revealed a positive relationship between purple urchin density and both the number and richness of fish predators, but these correlations were not observed when red urchins were present. Our results demonstrate highly variable mortality rates across prey densities in this system and suggest that top-down control of urchins can occur only under limited circumstances. Our findings provide insight into the dynamics of alternate community states observed on rocky reefs.

Eelgrass structural complexity mediates mesograzer herbivory on epiphytic algae.

Structural complexity mediates ecological processes such as predation, competition, and recruitment in marine systems, but relatively little is known about its effects on herbivory. In temperate seagrasses, such as eelgrass (Zostera marina), the primary herbivores are small crustacean and gastropod mesograzers that promote seagrass persistence by preferentially consuming competing epiphytic algae. We used a laboratory grazing experiment, a field colonization experiment, and stable isotope analysis to determine whether one component of eelgrass structural complexity, shoot density, dictates the strength of mesograzer top-down effects on epiphytic algae, and whether this is influenced by mesograzer community composition. Our results suggest that increasing structural complexity shifted eelgrass communities from a bottom-up to a top-down controlled system. In the lab, mesograzers reduced epiphyte standing stock only in high-shoot density experimental communities, though grazing impact varied among different combinations of dominant mesograzer taxa. In our field experiment, epiphyte biomass was inversely correlated with mesograzer density in high but not in low-shoot density eelgrass plots. High-shoot density plots contained lower epiphyte biomass despite housing lower densities of mesograzers, when compared to low-density plots, suggesting potential effects of mesograzer behavior, community composition, or self-shading on epiphyte growth. Our results suggest that structural complexity can strongly influence rates of top-down and bottom-up processes in eelgrass habitat, and should be incorporated into future experiments on the role of herbivores in seagrass ecosystems.

Interactive effects of predator and prey harvest on ecological resilience of rocky reefs.

A major goal of ecosystem-based fisheries management is to prevent fishery-induced shifts in community states. This requires an understanding of ecological resilience: the ability of an ecosystem to return to the same state following a perturbation, which can strongly depend on species interactions across trophic levels. We use a structured model of a temperate rocky reef to explore how multi-trophic level fisheries impact ecological resilience. Increasing fishing mortality of prey (urchins) has a minor effect on equilibrium biomass of kelp, urchins, and spiny lobster predators, but increases resilience by reducing the range of predator harvest rates at which alternative stable states are possible. Size-structured predation on urchins acts as the feedback maintaining each state. Our results demonstrate that the resilience of ecosystems strongly depends on the interactive effects of predator and prey harvest in multi-trophic level fisheries, which are common in marine ecosystems but are unaccounted for by traditional management.

Structural complexity and fish body size interactively affect habitat optimality.

Predator-prey interactions are strongly influenced by habitat structure, particularly in coastal marine habitats such as seagrasses in which structural complexity (SC) may vary over small spatial scales. For seagrass mesopredators such as juvenile fishes, optimality models predict that fitness will be maximized at levels of SC that enhance foraging but minimize predation risk, both of which are functions of body size. We tested the hypothesis that in eelgrass (Zostera marina) habitat, optimal SC for juvenile giant kelpfish (Heterostichus rostratus), an abundant eelgrass mesopredator in southern California, changes through ontogeny. To do this, we quantified eelgrass SC effects on habitat associations, relative predation risk, and foraging efficiency for three size classes of juvenile giant kelpfish. We found that habitat selection differed with fish size: small fish selected dense eelgrass, whereas larger fish selected sparse eelgrass. Small kelpfish experienced the lowest relative predation risk in dense eelgrass but also had higher foraging efficiency in dense eelgrass, suggesting that dense eelgrass is selected by these fish because it minimizes risk and maximizes potential for growth. Surprisingly, larger kelpfish did not experience lower predation risk than small kelpfish. However, larger kelpfish experienced higher foraging efficiency in sparse eelgrass vs. dense eelgrass, suggesting that they select sparse eelgrass to maximize foraging efficiency. Our study highlights that trade-offs between predation risk and foraging can occur within a single habitat type, that studies should consider how habitat value changes through ontogeny, and that seagrass habitat value may be maximal when within-patch variability in SC is high.

Invasive prey indirectly increase predation on their native competitors.

Ecological theory predicts that invasive prey can interact with native prey directly by competing for shared resources or indirectly by changing the abundance or behavior of shared native predators. However, both the study and management of invasive prey have historically overlooked indirect effects. In southern California estuaries, introduction of the Asian nest mussel Arcuatula senhousia has been linked to profound changes in native bivalve assemblages, but the mechanisms of these interactions remain unclear. We performed three field experiments to assess the mechanisms of competition between Arcuatula and native bivalves, and evaluated the potential for Arcuatula to indirectly mediate native predator-prey dynamics. We found that Arcuatula reduces the diversity, abundance, and size of native bivalve recruits by preemptively exploiting space in surface sediments. When paired with native shallow-dwelling clams (Chione undatella and Laevicardium substriatum), Arcuatula reduces adult survival through overgrowth competition. However, Arcuatula also attracts native predators, causing apparent competition by indirectly increasing predation of native clams, especially for poorly defended species. Therefore, invasive prey can indirectly increase predation rates on native competitors by changing the behavior of shared native predators, but the magnitude of apparent competition strongly depends on the vulnerability of natives to predation. Interestingly, our results indicate that the vulnerability of invasive prey to predation can greatly exacerbate impacts on their native competitors. Our findings suggest that consideration of both direct and indirect effects of invasive prey, as well as native predator-prey relationships, should lead to more effective invasive species management.

Disturbance facilitates the coexistence of antagonistic ecosystem engineers in California estuaries.

Ecological theory predicts that interactions between antagonistic ecosystem engineers can lead to local competitive exclusion, but disturbance can facilitate broader coexistence. However, few empirical studies have tested the potential for disturbance to mediate competition between engineers. We examined the capacity for disturbance and habitat modification to explain the disjunct distributions of two benthic ecosystem engineers, eelgrass Zostera marina and the burrowing ghost shrimp Neotrypaea californiensis, in two California estuaries. Sediment sampling in eelgrass and ghost shrimp patches revealed that ghost shrimp change benthic biogeochemistry over small scales (centimeters) but not patch scales (meters to tens of meters), suggesting a limited capacity for sediment modification to explain species distributions. To determine the relative competitive abilities of engineers, we conducted reciprocal transplantations of ghost shrimp and eelgrass. Local ghost shrimp densities declined rapidly following the addition of eelgrass, and transplanted eelgrass expanded laterally into the surrounding ghost shrimp-dominated areas. When transplanted into eelgrass patches, ghost shrimp failed to persist. Ghost shrimp were also displaced from plots with structural mimics of eelgrass rhizomes and roots, suggesting that autogenic habitat modification by eelgrass is an important mechanism determining ghost shrimp distributions. However, ghost shrimp were able to rapidly colonize experimental disturbances to eelgrass patch edges, which are common in shallow estuaries. We conclude that coexistence in this system is maintained by spatiotemporally asynchronous disturbances and a competition-colonization trade-off: eelgrass is a competitively superior ecosystem engineer, but benthic disturbances permit the coexistence of ghost shrimp at the landscape scale by modulating the availability of space.

Joint effects of patch edges and habitat degradation on faunal predation risk in a widespread marine foundation species.

Human activities degrade and fragment coastal marine habitats, reducing their structural complexity and making habitat edges a prevalent seascape feature. Though habitat edges frequently are implicated in reduced faunal survival and biodiversity, results of experiments on edge effects have been inconsistent, calling for a mechanistic approach to the study of edges that explicitly includes indirect and interactive effects of habitat alteration at multiple scales across biogeographic gradients. We used an experimental network spanning 17 eelgrass (Zostera marina) sites across the Atlantic and Pacific oceans and the Mediterranean Sea to determine (1) if eelgrass edges consistently increase faunal predation risk, (2) whether edge effects on predation risk are altered by habitat degradation (shoot thinning), and (3) whether variation in the strength of edge effects among sites can be explained by biogeographical variability in covarying eelgrass habitat features. Contrary to expectations, at most sites, predation risk for tethered crustaceans (crabs or shrimps) was lower along patch edges than in patch interiors, regardless of the extent of habitat degradation. However, the extent to which edges reduced predation risk, compared to the patch interior, was correlated with the extent to which edges supported higher eelgrass structural complexity and prey biomass compared to patch interiors. This suggests an indirect component to edge effects in which the impact of edge proximity on predation risk is mediated by the effect of edges on other key biotic factors. Our results suggest that studies on edge effects should consider structural characteristics of patch edges, which may vary geographically, and multiple ways that humans degrade habitats.

3D genomics across the tree of life reveals condensin II as a determinant of architecture type.

We investigated genome folding across the eukaryotic tree of life. We find two types of three-dimensional (3D) genome architectures at the chromosome scale. Each type appears and disappears repeatedly during eukaryotic evolution. The type of genome architecture that an organism exhibits correlates with the absence of condensin II subunits. Moreover, condensin II depletion converts the architecture of the human genome to a state resembling that seen in organisms such as fungi or mosquitoes. In this state, centromeres cluster together at nucleoli, and heterochromatin domains merge. We propose a physical model in which lengthwise compaction of chromosomes by condensin II during mitosis determines chromosome-scale genome architecture, with effects that are retained during the subsequent interphase. This mechanism likely has been conserved since the last common ancestor of all eukaryotes.

Effects of habitat patchiness on American lobster movement across a gradient of predation risk and shelter competition.

The influence of landscape structure on marine ecological processes is receiving increasing attention. However, few studies conducted in coastal marine habitats have evaluated whether the effects of landscape structure on species interactions and organismal behavior are consistent across the range of an organism, over which landscape context and the strength of species interactions typically vary. American lobster (Homarus americanus) juveniles seek refuge from predators within shallow rocky habitat but make short-distance movements to forage outside of shelter. We evaluated how the patchiness of cobble habitat influences juvenile lobster movement by conducting mark-recapture experiments on lobsters placed within patchy and contiguous cobble plots in three regions of New England among which risk of predation and intraspecific shelter competition vary (Rhode Island, mid-coast Maine, and eastern Maine, USA). We also evaluated whether habitat patchiness influenced lobster colonization of plots and whether lobster fidelity to individual shelters corresponds to variability in predator abundance and conspecific density among regions. Cobble patchiness reduced rates of lobster movement in all three regions in 2004 and in two of three regions in 2005, despite large differences in landscape context among regions. Region had much larger effects on lobster colonization than did patchiness, but patchy plots were colonized at higher rates than were contiguous plots where lobster densities were highest. Fidelity to shelter was higher in regions with low conspecific density (Rhode Island and eastern Maine) than in mid-coast Maine where conspecific density is high and where unmarked lobsters often occupied shelters vacated by marked lobsters. Our results indicate that cobble patchiness influences juvenile lobster movement at small scales, but that the effects of patchiness on movement were consistent across much of the range of the American lobster despite strong regional variation in predator abundance and conspecific density.

Biotic resistance to invasion along an estuarine gradient.

Biotic resistance is the ability of native communities to repel the establishment of invasive species. Predation by native species may confer biotic resistance to communities, but the environmental context under which this form of biotic resistance occurs is not well understood. We evaluated several factors that influence the distribution of invasive Asian mussels (Musculista senhousia) in Mission Bay, a southern California estuary containing an extensive eelgrass (Zostera marina) habitat. Asian mussels exhibit a distinct spatial pattern of invasion, with extremely high densities towards the back of Mission Bay (up to 4,000 m(-2)) in contrast with near-complete absence at sites towards the front of the bay. We established that recruits arrived at sites where adult mussels were absent and found that dense eelgrass does not appear to preclude Asian mussel growth and survival. Mussel survival and growth were high in predator-exclusion plots throughout the bay, but mussel survival was low in the front of the bay when plots were open to predators. Additional experiments revealed that consumption by spiny lobsters (Panulirus interruptus) and a gastropod (Pteropurpura festiva) likely are the primary factors responsible for resistance to Asian mussel invasion. However, biotic resistance was dependent on location within the estuary (for both species) and also on the availability of a hard substratum (for P. festiva). Our findings indicate that biotic resistance in the form of predation may be conferred by higher order predators, but that the strength of resistance may strongly vary across estuarine gradients and depend on the nature of the locally available habitat.