Eric Sanford

Top-down and bottom-up regulation of New Zealand rocky intertidal communities

Studies on the west coast of North America suggest that nearshore oceanographic conditions can have important effects on rocky intertidal community structure and dynamics. Specifically, upwelling-dependent processes in coastal waters can affect both top-down and bottom-up processes on adjacent rocky shores. As a first step in testing the prediction that similar linkages occur elsewhere, we investigated the effects and rates of predation, grazing, and recruitment on rocky intertidal community dynamics at upwelling and non-upwelling sites on the South Island of New Zealand. Comparative-experimental studies were done at each of two sites on both the east and west coasts of the South Island. We quantified benthic community structure, maximal wave force, nearshore sea-surface temperature, air temperature at low tide, nutrient concentrations, survival of mussels, rates and effects of predation, rates and effects of limpet grazing, recruitment of mussels and barnacles, and RNA:DNA ratios (a growth index) of muss...

Evolutionary change during experimental ocean acidification

Rising atmospheric carbon dioxide (CO2) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth’s oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO2 levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO2 levels. Although larval development and morphology showed little response to elevated CO2, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis—gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.

Functional impacts of ocean acidification in an ecologically critical foundation species

SUMMARY Anthropogenic CO2 is reducing the pH and altering the carbonate chemistry of seawater, with repercussions for marine organisms and ecosystems. Current research suggests that calcification will decrease in many species, but compelling evidence of impaired functional performance of calcium carbonate structures is sparse, particularly in key species. Here we demonstrate that ocean acidification markedly degrades the mechanical integrity of larval shells in the mussel Mytilus californianus, a critical community member on rocky shores throughout the northeastern Pacific. Larvae cultured in seawater containing CO2 concentrations expected by the year 2100 (540 or 970 ppm) precipitated weaker, thinner and smaller shells than individuals raised under present-day seawater conditions (380 ppm), and also exhibited lower tissue mass. Under a scenario where mussel larvae exposed to different CO2 levels develop at similar rates, these trends suggest a suite of potential consequences, including an exacerbated vulnerability of new settlers to crushing and drilling attacks by predators; poorer larval condition, causing increased energetic stress during metamorphosis; and greater risks from desiccation at low tide due to shifts in shell area to body mass ratios. Under an alternative scenario where responses derive exclusively from slowed development, with impacted individuals reaching identical milestones in shell strength and size by settlement, a lengthened larval phase could increase exposure to high planktonic mortality rates. In either case, because early life stages operate as population bottlenecks, driving general patterns of distribution and abundance, the ecological success of this vital species may be tied to how ocean acidification proceeds in coming decades.

Water Temperature, Predation, and the Neglected Role of Physiological Rate Effects in Rocky Intertidal Communities

Abstract Ecologists and physiologists working on rocky shores have emphasized the effects of environmental stress on the distribution of intertidal organisms. Although consumer stress models suggest that physical extremes may often reduce predation and herbivory through negative impacts on the physiological performance of consumers, few field studies have rigorously tested how environmental variation affects feeding rates. I review and analyze field experiments that quantified per capita feeding rates of a keystone predator, the sea star Pisaster ochraceus, in relation to aerial heat stress, wave forces, and water temperature at three rocky intertidal sites on the Oregon coast. Predation rates during 14-day periods were unrelated to aerial temperature, but decreased significantly with decreasing water temperature. There was suggestive but inconclusive evidence that predation rates also declined with increasing wave forces. Data-logger records suggested that thermal stress was rare in the wave-exposed habitats that I studied; sea star body temperatures likely reached warm levels (>24°C) on only 9 dates in 3 yr. In contrast, wind-driven upwelling regularly generated 3 to 5°C fluctuations in water temperature, and field and laboratory results suggest that such changes significantly alter feeding rates of Pisaster. These physiological rate effects, near the center of an organisms thermal range, may not reduce growth or fitness, and thus are distinct from the effects of environmental stress. This study underscores the need to consider organismal responses both under “normal” conditions, as well as under extreme conditions. Examining both kinds of responses is necessary to understand how different components of environmental variation regulate physiological performance and the strength of species interactions in intertidal communities.

The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling

Although most upwelling regions are marked by strong fluctuations in water temperature, few studies have examined how episodic cold-water events affect the physiology and ecology of benthic marine invertebrates. I tested the hypothesis that upwelling-related variation in water temperature regulates the feeding, growth, and energetics of two rocky intertidal predators, the sea star Pisaster ochraceus (Brandt, 1835) and the whelk Nucella canaliculata (Duclos, 1832). Sea stars and whelks were maintained in laboratory tanks at a constant 9 °C, a constant 12 °C, and a treatment that simulated the Oregon coast upwelling regime by cycling between 14-day periods of 12 and 9 °C. Early in the experiments, sea stars and whelks held at 9 °C consumed about 30% fewer mussels (Mytilus trossulus) than those in warmer tanks. Despite lower consumption by whelks in colder tanks, 9 and 12 °C individuals attained the same final size. Similarly, sea stars in 9 °C tanks showed greater growth per gram of mussel tissue consumed than individuals held at 12 °C. These results suggest that reduced consumption under colder conditions was balanced by reduced metabolic costs. Moreover, there appeared to be an energetic advantage to living in the temperature regime characteristic of intermittent upwelling. Sea stars alternately exposed to 12 and 9 °C had a significantly higher growth rate, conversion efficiency, and storage of reserves in the pyloric caeca than individuals in the constant 12 °C tanks. Whelks maintained under fluctuating temperatures tended to grow faster than those held at constant 12 or 9 °C, although this trend was not statistically significant (p=0.069). These results suggest that benthic consumers experiencing cyclic temperatures may feed intensely during periods of warmer water while benefiting from reduced metabolic costs during cold-water intrusions. Because the fecundity of Pisaster and Nucella is a function of energy stored during the upwelling season, interannual variability in upwelling patterns could alter the reproductive output of these species.

Inter-hemispheric comparison of bottom-up effects on community structure: Insights revealed using the comparative-experimental approach

The comparative-experimental approach uses identically designed, replicated experiments at different sites along environmental gradients in order to gain insight into the changing dynamics of communities with changing environmental conditions. Such studies reveal how ecological processes vary in intensity and interact to produce community structure. Early emphases were on the community consequences of shifting top-down impacts, competition and disturbance with environmental stress. Recent advances include the more precise quantification of gradients and thus a better understanding of species responses to the environment, and the revelation that bottom-up forces can vary significantly on within-region scales, with major consequences for the impact of top-down forces and thus community dynamics. Here the use of the method to examine the role of geographic location (coastal ecosystems in different hemispheres) and oceanographic conditions (upwelling vs downwelling) on these bottom-up/top-down linkages is advanced. We show that a bottom-up factor (prey recruitment) and a top-down effect (predation rate) vary consistently with oceanographic conditions within each coastal ecosystem, and also between geographic locations (New Zealand, Oregon). In general, both recruitment and predation rates are higher in Oregon. It is postulated that these differences are common responses to oceanographic variation, and that between-hemisphere differences result from the stronger and more persistent upwelling in the California Current ecosystem.

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails.

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO2, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO2 experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO2 oysters were consumed. The invasive snails were tolerant of elevated CO2 with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.

Population genetic analysis of a recent range expansion: mechanisms regulating the poleward range limit in the volcano barnacle Tetraclita rubescens

As range shifts coincident with climate change have become increasingly well documented, efforts to describe the causes of range boundaries have increased. Three mechanisms—genetic impoverishment, migration load, or a physical barrier to dispersal—are well described theoretically, but the data needed to distinguish among them have rarely been collected. We describe the distribution, abundance, genetic variation, and environment of Tetraclita rubescens, an intertidal barnacle that expanded its northern range limit by several hundreds of kilometres from San Francisco, CA, USA, since the 1970s. We compare geographic variation in abundance with abiotic and biotic patterns, including sea surface temperatures and the distributions of 387 co‐occurring species, and describe genetic variation in cytochrome c oxidase subunit I, mitochondrial noncoding region, and nine microsatellite loci from 27 locations between Bahia Magdalena (California Baja Sur, Mexico) and Cape Mendocino (CA, USA). We find very high gene flow, high genetic diversity, and a gradient in physical environmental variation coincident with the range limit. We infer that the primary cause of the northern range boundary in T. rubescens is migration load arising from flow of maladapted alleles into peripheral locations and that environmental change, which could have reduced selection against genotypes immigrating into the newly colonized portion of the range, is the most likely cause of the observed range expansion. Because environmental change could similarly affect all taxa in a region whose distributional limits are established by migration load, these mechanisms may be common causes of range boundaries and largely synchronous multi‐species range expansions.

Natural History Note An Intertidal Sea Star Adjusts Thermal Inertia to Avoid Extreme Body Temperatures

The body temperature of ectotherms is influenced by the interaction of abiotic conditions, morphology, and behavior. Although organisms living in different thermal habitats may exhibit morphological plasticity or move from unfavorable locations, there are few examples of animals adjusting their thermal properties in response to short‐term changes in local conditions. Here, we show that the intertidal sea star Pisaster ochraceus modulates its thermal inertia in response to prior thermal exposure. After exposure to high body temperature at low tide, sea stars increase the amount of colder‐than‐air fluid in their coelomic cavity when submerged during high tide, resulting in a lower body temperature during the subsequent low tide. Moreover, this buffering capacity is more effective when seawater is cold during the previous high tide. This ability to modify the volume of coelomic fluid provides sea stars with a novel thermoregulatory “backup” when faced with prolonged exposure to elevated aerial temperatures.

Predicting the Effects of Ocean Acidification on Predator-Prey Interactions: A Conceptual Framework Based on Coastal Molluscs

The influence of environmental change on species interactions will affect population dynamics and community structure in the future, but our current understanding of the outcomes of species interactions in a high-CO2 world is limited. Here, we draw upon emerging experimental research examining the effects of ocean acidification on coastal molluscs to provide hypotheses of the potential impacts of high-CO2 on predator-prey interactions. Coastal molluscs, such as oysters, mussels, and snails, allocate energy among defenses, growth, and reproduction. Ocean acidification increases the energetic costs of physiological processes such as acid-base regulation and calcification. Impacted molluscs can display complex and divergent patterns of energy allocation to defenses and growth that may influence predator-prey interactions; these include changes in shell properties, body size, tissue mass, immune function, or reproductive output. Ocean acidification has also been shown to induce complex changes in chemoreception, behavior, and inducible defenses, including altered cue detection and predator avoidance behaviors. Each of these responses may ultimately alter the susceptibility of coastal molluscs to predation through effects on predator handling time, satiation, and search time. While many of these effects may manifest as increases in per capita predation rates on coastal molluscs, the ultimate outcome of predator-prey interactions will also depend on how ocean acidification affects the specified predators, which also exhibit complex responses to ocean acidification. Changes in predator-prey interactions could have profound and unexplored consequences for the population dynamics of coastal molluscs in a high-CO2 ocean.