Brent B. Hughes

Reproductive longevity of drifting kelp Macrocystis pyrifera (Phaeophyceae) in Monterey Bay

Drifting Macrocystis pyrifera (L.) C. Agardh sporophytes have long been viewed as the primary long‐distance dispersal vector; yet, few data exist that support the ability of reproductive viable sporophytes to actually travel the presumed hundreds to thousands of kilometers. This study addressed the reproductive longevity of experimental and naturally occurring M. pyrifera drifters. Temporal variability in sporophyte size and reproduction was estimated for experimental drifting sporophytes that were tethered to surface buoys and compared with attached plants (controls). Reproductive viability was also studied for beach‐cast drifters (BCD), and naturally drifting sporophytes observed during field surveys in Monterey Bay. Detached drifting sporophytes were tracked with radio transmitters to follow drifter trajectories and to measure drifting speed. Experimental drifters (ED) experienced a 74% reduction in frond length after 35 days, a 76% reduction in average frond number after 70 days, and a reduction in average sorus area by 83% after 28 days. Although zoospore production was reduced following detachment, sporophytes remained fertile with high zoospore germination success as long as sori were present (125 days). Zoospore production and germination success for natural and BCD was similar to ED. The average displacement of radio‐tagged drifters was 7.12 km·day−1, suggesting that a sporophyte adrift for 125 days disperses viable propagules (zoospores) over 890 km (±363). Dispersal of propagules is important for population restoration, distribution, and genetic diversity. Such dispersal distances are long enough to connect potentially all Northern Hemisphere Macrocystis populations across a generational timescale and may facilitate inter‐hemispheric gene flow.

Recovery of a top predator mediates negative eutrophic effects on seagrass

Significance Many coastal vegetated ecosystems have declined, affected by human alterations to “bottom-up” forces such as nutrient loading from agriculture and by “top-down” forces such as overfishing of predators. Examining the interactions between such bottom-up and top-down changes is challenging, because top predators have disappeared from many of these ecosystems. A highly nutrient-loaded estuary in California recently colonized by a recovering sea otter population provided an unusual opportunity to examine these interactions. We demonstrate that top-down effects of sea otters mitigate negative effects of nutrient loading, enhancing growth of seagrass. Grazers that remove algae from seagrass are favored by decreased crabs resulting from otter predation. Recovery of top predators can thus support resilience of coastal vegetated ecosystems. A fundamental goal of the study of ecology is to determine the drivers of habitat-forming vegetation, with much emphasis given to the relative importance to vegetation of “bottom-up” forces such as the role of nutrients and “top-down” forces such as the influence of herbivores and their predators. For coastal vegetation (e.g., kelp, seagrass, marsh, and mangroves) it has been well demonstrated that alterations to bottom-up forcing can cause major disturbances leading to loss of dominant vegetation. One such process is anthropogenic nutrient loading, which can lead to major changes in the abundance and species composition of primary producers, ultimately affecting important ecosystem services. In contrast, much less is known about the relative importance of apex predators on coastal vegetated ecosystems because most top predator populations have been depleted or lost completely. Here we provide evidence that an unusual four-level trophic cascade applies in one such system, whereby a top predator mitigates the bottom-up influences of nutrient loading. In a study of seagrass beds in an estuarine ecosystem exposed to extreme nutrient loading, we use a combination of a 50-y time series analysis, spatial comparisons, and mesocosm and field experiments to demonstrate that sea otters (Enhydra lutris) promote the growth and expansion of eelgrass (Zostera marina) through a trophic cascade, counteracting the negative effects of agriculturally induced nutrient loading. Our results add to a small but growing body of literature illustrating that significant interactions between bottom-up and top-down forces occur, in this case with consequences for the conservation of valued ecosystem services provided by seagrass.

Long-Term Studies Contribute Disproportionately to Ecology and Policy

Abstract As the contribution for long‐term ecological and environmental studies (LTEES) to our understanding of how species and ecosystems respond to a changing global climate becomes more urgent, the relative number and investment in LTEES are declining. To assess the value of LTEES to advancing the field of ecology, we evaluated relationships between citation rates and study duration, as well as the representation of LTEES with the impact factors of 15 ecological journals. We found that the proportionate representation of LTEES increases with journal impact factor and that the positive relationship between citation rate and study duration is stronger as journal impact factor increases. We also found that the representation of LTEES in reports written to inform policy was greater than their representation in the ecological literature and that their authors particularly valued LTEES. We conclude that the relative investment in LTEES by ecologists and funders should be seriously reconsidered for advancing ecology and its contribution to informing environmental policy.

Climate mediates hypoxic stress on fish diversity and nursery function at the land–sea interface

Significance Human populations are rapidly expanding along Earths coastlines, increasing stress to coastal ecosystems and the services they provide. One of these stressors comes from an increase in nutrient inputs from coastal land development that can enter estuaries and coastal seas leading to algal blooms that deplete oxygen from the water, a condition known as hypoxia. In this study, we investigated how coastal hypoxia influences fish diversity, the nursery habitat for juvenile fish, and fisheries production in adjacent offshore waters. We found that severity in hypoxia corresponded with declines to fish diversity, nursery quality, and offshore fisheries. Furthermore, intensification of El Niño mediated hypoxia by improving dissolved oxygen conditions, demonstrating that climate can influence anthropogenic stressors affecting coastal ecosystem services. Coastal ecosystems provide numerous important ecological services, including maintenance of biodiversity and nursery grounds for many fish species of ecological and economic importance. However, human population growth has led to increased pollution, ocean warming, hypoxia, and habitat alteration that threaten ecosystem services. In this study, we used long-term datasets of fish abundance, water quality, and climatic factors to assess the threat of hypoxia and the regulating effects of climate on fish diversity and nursery conditions in Elkhorn Slough, a highly eutrophic estuary in central California (United States), which also serves as a biodiversity hot spot and critical nursery grounds for offshore fisheries in a broader region. We found that hypoxic conditions had strong negative effects on extent of suitable fish habitat, fish species richness, and abundance of the two most common flatfish species, English sole (Parophrys vetulus) and speckled sanddab (Citharichthys stigmaeus). The estuary serves as an important nursery ground for English sole, making this species vulnerable to anthropogenic threats. We determined that estuarine hypoxia was associated with significant declines in English sole nursery habitat, with cascading effects on recruitment to the offshore adult population and fishery, indicating that human land use activities can indirectly affect offshore fisheries. Estuarine hypoxic conditions varied spatially and temporally and were alleviated by strengthening of El Niño conditions through indirect pathways, a consistent result in most estuaries across the northeast Pacific. These results demonstrate that changes to coastal land use and climate can fundamentally alter the diversity and functioning of coastal nurseries and their adjacent ocean ecosystems.

Trophic cascades on the edge: fostering seagrass resilience via a novel pathway

Despite widespread degradation, some coastal ecosystems display remarkable resilience. For seagrasses, a century-old paradigm has implicated macroalgal blooms stimulated by anthropogenic nutrient, loading as a primary driver of seagrass decline, yet relatively little attention has been given to drivers of seagrass resilience. In Elkhorn Slough, CA, an estuarine system characterized by extreme anthropogenic nutrient loading and macroalgal (Ulva spp.) blooms, seagrass (Zostera marina) beds have recovered concurrent with colonization of the estuary by top predators, sea otters (Enhydra lutris). Here, we follow up on the results of a previous experiment at the seagrass interior, showing how sea otters can generate a trophic cascade that promotes seagrass. We conducted an experiment and constructed structural equation models to determine how sea otters, through a trophic cascade, might affect the edge of seagrass beds where expansion occurs. We found that at the edge, sea otters promoted both seagrass and ephemeral macroalgae, with the latter contributing beneficial grazers to the seagrass. The surprising results that sea otters promote two potentially competing vegetation types, and a grazer assemblage at their boundary provides a mechanism by which seagrasses can expand in eutrophic environments, and contributes to a growing body of literature demonstrating that ephemeral macroalgae are not always negatively associated with seagrass. Our results highlight the potential for top predator recovery to enhance ecosystem resilience to anthropogenic alterations through several cascading mechanisms.

Thresholds in marsh resilience to the Deepwater Horizon oil spill

Ecosystem boundary retreat due to human-induced pressure is a generally observed phenomenon. However, studies that document thresholds beyond which internal resistance mechanisms are overwhelmed are uncommon. Following the Deepwater Horizon (DWH) oil spill, field studies from a few sites suggested that oiling of salt marshes could lead to a biogeomorphic feedback where plant death resulted in increased marsh erosion. We tested for spatial generality of and thresholds in this effect across 103 salt marsh sites spanning ~430 kilometers of shoreline in coastal Louisiana, Alabama, and Mississippi, using data collected as part of the natural resource damage assessment (NRDA). Our analyses revealed a threshold for oil impacts on marsh edge erosion, with higher erosion rates occurring for ~1–2 years after the spill at sites with the highest amounts of plant stem oiling (90–100%). These results provide compelling evidence showing large-scale ecosystem loss following the Deepwater Horizon oil spill. More broadly, these findings provide rare empirical evidence identifying a geomorphologic threshold in the resistance of an ecosystem to increasing intensity of human-induced disturbance.

Unexpected resilience of a seagrass system exposed to global stressors

Despite a growing interest in identifying tipping points in response to environmental change, our understanding of the ecological mechanisms underlying nonlinear ecosystem dynamics is limited. Ecosystems governed by strong species interactions can provide important insight into how nonlinear relationships between organisms and their environment propagate through ecosystems, and the potential for environmentally mediated species interactions to drive or protect against sudden ecosystem shifts. Here, we experimentally determine the functional relationships (i.e., the shapes of the relationships between predictor and response variables) of a seagrass assemblage with well-defined species interactions to ocean acidification (enrichment of CO2 ) in isolation and in combination with nutrient loading. We demonstrate that the effect of ocean acidification on grazer biomass (Phyllaplysia taylori and Idotea resecata) was quadratic, with the peak of grazer biomass at mid-pH levels. Algal grazing was negatively affected by nutrients, potentially due to low grazer affinity for macroalgae (Ulva intestinalis), as recruitment of both macroalgae and diatoms were favored in elevated nutrient conditions. This led to an exponential increase in macroalgal and epiphyte biomass with ocean acidification, regardless of nutrient concentration. When left unchecked, algae can cause declines in seagrass productivity and persistence through shading and competition. Despite quadratic and exponential functional relationships to stressors that could cause a nonlinear decrease in seagrass biomass, productivity of our model seagrass-the eelgrass (Zostera marina)- remained highly resilient to increasing acidification. These results suggest that important species interactions governing ecosystem dynamics may shift with environmental change, and ecosystem state may be decoupled from ecological responses at lower levels of organization.

Effects of Hypoxia on Fish Survival and Oyster Growth in a Highly Eutrophic Estuary

Human land use activities around estuaries can result in high levels of eutrophication. At Elkhorn Slough estuary, a highly eutrophic California estuary, we investigated the effects of impaired water quality on two stress-tolerant estuarine species, a common fish, the staghorn sculpin, Leptocottus armatus and a foundational invertebrate, the Olympia oyster, Ostrea lurida. We caged the two indicator species at six wetlands with different levels of water quality impairment, four of which had restricted tidal flow. We also recorded water quality parameters simultaneously at all sites using YSI sondes, and sampled nutrients and chlorophyll-a monthly, building on the National Estuarine Research Reserve System-wide Monitoring Program. We found that the monitored environmental variables predicted ecological responses by the indicator species. In particular, we found that the duration and severity of hypoxia were negatively correlated with fish survival and oyster growth. Further, our results corroborate previous studies that artificial tidal restriction leads to increased hypoxia stress. We conclude that large diurnal fluctuations in dissolved oxygen and extended nighttime hypoxia can have lethal and sub-lethal effects even on stress-tolerant organisms in the estuary. While laboratory experiments have often shown such effects, it is relatively rare to demonstrate negative effects of oxygen variation with in situ experiments, which provide stakeholders with concrete evidence for impaired water quality at local wetlands. Tidally restricted sites, which experience the largest fluctuations in dissolved oxygen and longest periods of hypoxia, harbor conditions harmful to vertebrates and invertebrates in the estuary. Reversing the anthropogenically induced low oxygen levels, by restoring more natural tidal exchange and by decreasing agricultural runoff, could improve the survival and growth of important estuarine organisms.

Are seagrass beds indicators of anthropogenic nutrient stress in the rocky intertidal

It is well established that anthropogenic nutrient inputs harm estuarine seagrasses, but the influence of nutrients in rocky intertidal ecosystems is less clear. In this study, we investigated the effect of anthropogenic nutrient loading on Phyllospadix spp., a rocky intertidal seagrass, at local and regional scales. At sites along California, Washington, and Oregon, we demonstrated a significant, negative correlation of urban development and Phyllospadix bed thickness. These results were echoed locally along an urban gradient on the central California coast, where Phyllospadix shoot δ15N was negatively associated with Phyllospadix bed thickness, and experimentally, where nutrient additions in mesocosms reduced Phyllospadix shoot formation and increased epiphytic cover on Phyllospadix shoots. These findings provide evidence that coastal development can threaten rocky intertidal seagrasses through increased epiphytism. Considering that seagrasses provide vital ecosystem services, mitigating eutrophication and other factors associated with development in the rocky intertidal coastal zone should be a management priority.

Ecosystem features determine seagrass community response to sea otter foraging

Comparing sea otter recovery in California (CA) and British Columbia (BC) reveals key ecosystem properties that shape top-down effects in seagrass communities. We review potential ecosystem drivers of sea otter foraging in CA and BC seagrass beds, including the role of coastline complexity and environmental stress on sea otter effects. In BC, we find greater species richness across seagrass trophic assemblages. Furthermore, Cancer spp. crabs, an important link in the seagrass trophic cascade observed in CA, are less common. Additionally, the more recent reintroduction of sea otters, more complex coastline, and reduced environmental stress in BC seagrass habitats supports the hypotheses that sea otter foraging pressure is currently reduced there. In order to manage the ecosystem features that lead to regional differences in top predator effects in seagrass communities, we review our findings, their spatial and temporal constraints, and present a social-ecological framework for future research.