Jake A. Lawlor & Shawn M. Arellano
Scientific Reports volume 10, Article number: 13787 (2020)
Most invertebrates in the ocean begin their lives with planktonic larval phases that are critical for dispersal and distribution of these species. Larvae are particularly vulnerable to environmental change, so understanding interactive effects of environmental stressors on larval life is essential in predicting population persistence and vulnerability of species. Here, we use a novel experimental approach to rear larvae under interacting gradients of temperature, salinity, and ocean acidification, then model growth rate and duration of Olympia oyster larvae and predict the suitability of habitats for larval survival. We find that temperature and salinity are closely linked to larval growth and larval habitat suitability, but larvae are tolerant to acidification at this scale. We discover that present conditions in the Salish Sea are actually suboptimal for Olympia oyster larvae from populations in the region, and that larvae from these populations might actually benefit from some degree of global ocean change. Our models predict a vast decrease in mean pelagic larval duration by the year 2095, which has the potential to alter population dynamics for this species in future oceans. Additionally, we find that larval tolerance can explain large-scale biogeographic patterns for this species across its range.
Many marine invertebrates begin their lives as tiny planktonic larvae that drift in the water column and disperse away from their parents. For sessile species, these larval periods are especially important as they are the only times throughout life history during which organisms are capable of dispersal. As such, survival during the larval phase is critical for the persistence of populations. Larvae are highly sensitive to environmental conditions and the vast majority of larvae do not live to competence, so population demographics and geographic distributions of species are closely related to patterns of larval survival and metamorphosis along environmental gradients. Thus, responses of early life-history stages to the environmental conditions in the larval habitat help to explain and predict the structures of communities in coastal oceans.
Understanding environmental influence on life-history bottlenecks is particularly important as climate variables that affect fitness are rapidly changing. Though the list of anthropogenically-influenced climate variables is broad and regionally variable, three of the most important environmental factors to consider are ocean temperature, acidification, and salinity. Broadly, temperature influences physiology of ectotherms, and thermal tolerances largely dictate distributions of marine organisms; changes in ocean temperature can cause changes in developmental rate and survival that delimit range boundaries of species. Acidification, or the shift of carbonate chemistry of a system, can affect calcification of animals with carbonate skeletons and, thus, will disproportionately affect many essential ecosystem engineers in marine systems such as corals, bivalves, and crabs. Changes in ocean salinity affect cellular processes such as osmotic regulation and respiration in marine animals, and sustained periods of low salinity can lead to mass die offs of intertidal populations. Further, these stressors interact in coastal environments, and impacts of combined stressors often operate synergistically, highlighting the importance of studying stressors in combination. By the year 2,100, climate models predict between 2 and 5 °C rise in sea surface temperatures, a pH drop of up to 0.4 pH units, and more frequent pulses of freshwater in coastal regions. Better understanding of how these changes will influence marine species is increasingly important for conservation and resource management in this time of rapid global change.
Oysters are pertinent models for climate change studies because they are calcifying invertebrates that depend solely on the larval phase for dispersal and they have immense ecological and economic importance. Here, we analyze interacting influences of temperature, salinity, and acidification on larvae of the Olympia oyster, Ostrea lurida. Once a major fishery on the U.S. West Coast, this species now exists at small fractions of its historical numbers due to decades of overharvesting, pollution, and habitat destruction. Now, Ostrea lurida is a species of key regional concern on the U.S. West Coast. In Washington state, the Department of Fish and Wildlife, in collaboration with Tribal governments and conservation NGOs, has identified 19 restoration sites for the species in the Salish Sea, with the goal of repopulating selected bays with self-sustaining Olympia oyster populations. Restoration efforts include out-planting of hatchery-raised seed into restoration sites, but further establishment of populations will rely on natural larval settlement. Predicting environments in which larvae can thrive will help to predict future success of populations and more precise targets for restoration efforts.
We tested the influence of environmental factors on growth rate and pelagic larval duration (PLD)—or the time between release and settlement—of O. lurida larvae, and on suitability of larval habitats to facilitate larval survival. In bivalves, we generally expect acidification to reduce larval growth rate and increase PLD, warming to reduce PLD but have variable effects on larval growth, and hyposalinity to decrease larval growth and increase PLD. Slower growth rates and longer PLDs may lead to lower survival but longer dispersal potential for these larvae, depending on their behaviors. Growth rate and PLD determine the timeframe over which larvae can access ocean currents for dispersal, thus, changes in these factors influence population connectivity as well. Further, the maximum extent of a species’ distribution in any given spawn season can be outlined by the suitability of the larval habitat for survival because larvae are more sensitive to environmental stress than adult stages. Certain habitat conditions may support adult oysters, but if those conditions do not support survival of larvae to competency, those habitats will fail as sources of viable larvae or as sites for new adult populations. For bivalves, we generally expect acidification, warming, and freshening to decrease larval habitat suitability, which may have broader implications for this species’ distribution in the future.
Interactions between stressors can be complex, and traditional multifactorial experimental designs are often limited by treatment value resolution, making it difficult to capture the full complexity of multidimensional functional response curves. Because conditions in the ocean do not occur in isolation or at discrete levels, we employ a novel experimental tank system to rear larvae in interacting gradients of environmental conditions. Using fifty unique experimental treatments of combined temperature, salinity, and acidification levels all housed in one tank, we test impacts of these variables on O. lurida larvae (Fig. 1). This unique design allows us to address continuous functional response patterns across environmental gradients while avoiding many issues of pseudoreplication associated with multi-factor studies. Using Generalized Additive and Generalized Linear Modeling of these experimental data, we predict larval growth and larval habitat suitability under current conditions in the Salish Sea, and as environmental conditions continue to change.