Biogeography of ocean acidification: Differential field performance of transplanted mussels to upwelling-driven variation in carbonate chemistry.

Ocean acidification (OA) represents a serious challenge to marine ecosystems. Laboratory studies addressing OA indicate broadly negative effects for marine organisms, particularly those relying on calcification processes. Growing evidence also suggests OA combined with other environmental stressors may be even more deleterious. Scaling these laboratory studies to ecological performance in the field, where environmental heterogeneity may mediate responses, is a critical next step toward understanding OA impacts on natural communities. We leveraged an upwelling-driven pH mosaic along the California Current System to deconstruct the relative influences of pH, ocean temperature, and food availability on seasonal growth, condition and shell thickness of the ecologically dominant intertidal mussel Mytilus californianus. In 2011 and 2012, ecological performance of adult mussels from local and commonly sourced populations was measured at 8 rocky intertidal sites between central Oregon and southern California. Sites coincided with a large-scale network of intertidal pH sensors, allowing comparisons among pH and other environmental stressors. Adult California mussel growth and size varied latitudinally among sites and inter-annually, and mean shell thickness index and shell weight growth were reduced with low pH. Surprisingly, shell length growth and the ratio of tissue to shell weight were enhanced, not diminished as expected, by low pH. In contrast, and as expected, shell weight growth and shell thickness were both diminished by low pH, consistent with the idea that OA exposure can compromise shell-dependent defenses against predators or wave forces. We also found that adult mussel shell weight growth and relative tissue mass were negatively associated with increased pH variability. Including local pH conditions with previously documented influences of ocean temperature, food availability, aerial exposure, and origin site enhanced the explanatory power of models describing observed performance differences. Responses of local mussel populations differed from those of a common source population suggesting mussel performance partially depended on genetic or persistent phenotypic differences. In light of prior research showing deleterious effects of low pH on larval mussels, our results suggest a life history transition leading to greater resilience in at least some performance metrics to ocean acidification by adult California mussels. Our data also demonstrate "hot" (more extreme) and "cold" (less extreme) spots in both mussel responses and environmental conditions, a pattern that may enable mitigation approaches in response to future changes in climate.

Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery.

Disease outbreaks can have substantial impacts on wild populations, but the often patchy or anecdotal evidence of these impacts impedes our ability to understand outbreak dynamics. Recently however, a severe disease outbreak occurred in a group of very well-studied organisms-sea stars along the west coast of North America. We analyzed nearly two decades of data from a coordinated monitoring effort at 88 sites ranging from southern British Columbia to San Diego, California along with 2 sites near Sitka, Alaska to better understand the effects of sea star wasting disease (SSWD) on the keystone intertidal predator, Pisaster ochraceus. Quantitative surveys revealed unprecedented declines of P. ochraceus in 2014 and 2015 across nearly the entire geographic range of the species. The intensity of the impact of SSWD was not uniform across the affected area, with proportionally greater population declines in the southern regions relative to the north. The degree of population decline was unrelated to pre-outbreak P. ochraceus density, although these factors have been linked in other well-documented disease events. While elevated seawater temperatures were not broadly linked to the initial emergence of SSWD, anomalously high seawater temperatures in 2014 and 2015 might have exacerbated the disease's impact. Both before and after the onset of the SSWD outbreak, we documented higher recruitment of P. ochraceus in the north than in the south, and while some juveniles are surviving (as evidenced by transition of recruitment pulses to larger size classes), post-SSWD survivorship is lower than during pre-SSWD periods. In hindsight, our data suggest that the SSWD event defied prediction based on two factors found to be important in other marine disease events, sea water temperature and population density, and illustrate the importance of surveillance of natural populations as one element of an integrated approach to marine disease ecology. Low levels of SSWD-symptomatic sea stars are still present throughout the impacted range, thus the outlook for population recovery is uncertain.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.

Detecting the unexpected: a research framework for ocean acidification.

The threat that ocean acidification (OA) poses to marine ecosystems is now recognized and U.S. funding agencies have designated specific funding for the study of OA. We present a research framework for studying OA that describes it as a biogeochemical event that impacts individual species and ecosystems in potentially unexpected ways. We draw upon specific lessons learned about ecosystem responses from research on acid rain, carbon dioxide enrichment in terrestrial plant communities, and nitrogen deposition. We further characterize the links between carbon chemistry changes and effects on individuals and ecosystems, and enumerate key hypotheses for testing. Finally, we quantify how U.S. research funding has been distributed among these linkages, concluding that there is an urgent need for research programs designed to anticipate how the effects of OA will reverberate throughout assemblages of species.

More than a meal integrating non-feeding interactions into food webs.

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.

Climate and recruitment of rocky shore intertidal invertebrates in the eastern North Atlantic.

Studies of the impacts of climate and climate change on biological systems often attempt to correlate ecological responses with basin-scale indices such as the North Atlantic Oscillation (NAO). However, such correlations, while useful for detecting long-term trends, are unable to provide a mechanism linking the physical environment and ecological processes. Here we evaluate the effects of the NAO on recruitment variability of rocky intertidal invertebrates in the North Atlantic examining two possible climate-related pathways. Using a highly conservative test we interpret associations with the NAO integrated over a season (three months) as an indicator of atmospheric effects on newly settled recruits (NAO3), and the effects of the NAO integrated over six months (NAO6) as an indicator of changes in ocean circulation affecting patterns of larval transport. Through an extensive literature survey we found 13 time series, restricted to southwest Ireland and Britain and comprising five species, that could be used for statistical analysis. Significant correlations with NAO3, our proxy for atmospheric effects, were observed in the south-central domain of our study region (southwest Ireland and south England). Significant correlations with NAO6, the proxy for ocean circulation effects, were detected on southwest Ireland. The associations were detected for three (two barnacles and a topshell) at two sites. These results suggest that the NAO can have effects on the recruitment of intertidal invertebrates through different pathways linked to climate and be distributed heterogeneously in space. Based on previous evidence and the sign and geographic location of significant correlations, we suggest that winter NAO effects are likely to occur as a result of effects on the survival of early life stages settling during spring or through changes in phenology. Our results argue that a combination of modeling and synthesis can be used to generate hypotheses regarding the effects of climate on recruitment and aid in the design of field-based tests of explicit ecological mechanisms.

Scales of dispersal and the biogeography of marine predator-prey interactions.

Striking differences in the dispersal of coexisting species have fascinated marine ecologists for decades. Despite widespread attention to the impact of dispersal on individual species dynamics, its role in species interactions has received comparatively little attention. Here, we approach the issue by combining analyses of simple heuristic predator-prey models with different dispersal patterns and data from several predator-prey systems from the Pacific coasts of North and South America. In agreement with model predictions, differences in predator dispersal generated characteristic biogeographic patterns. Predators lacking pelagic larvae tracked geographic variation in prey recruitment but not prey abundance. Prey recruitment rate alone explained more than 80% of the biogeographic variation in predator abundance. In contrast, predators with broadcasting larvae were uncorrelated with prey recruitment or adult prey abundance. Our findings reconcile perplexing results from previous studies and suggest that simple models can capture some of the complexity of life-history diversity in marine communities.

Climate change and latitudinal patterns of intertidal thermal stress.

The interaction of climate and the timing of low tides along the West Coast of the United States creates a complex mosaic of thermal environments, in which northern sites can be more thermally stressful than southern sites. Thus, climate change may not lead to a poleward shift in the distribution of intertidal organisms, as has been proposed, but instead will likely cause localized extinctions at a series of "hot spots." Patterns of exposure to extreme climatic conditions are temporally variable, and tidal predictions suggest that in the next 3 to 5 years "hot spots" are likely to appear at several northern sites.