Kelp-associated variability in seawater chemistry during a marine heatwave event connects to transgenerational effects in the purple urchin Strongylocentrotus purpuratus

Abstract

Giant kelp Macrocystis pyrifera provides the foundation for immense biodiversity on the coast of California, USA. Kelp forests can change seawater retention time, altering water chemistry, including pH and dissolved oxygen (DO), as well as the magnitude and predictability of variability in the same properties. Environmental heterogeneity across space and time could drive organismal performance and processes such as transgenerational plasticity (TGP), where parental experience modifies the offspring phenotype, potentially conferring tolerance to future environmental stress. We monitored environmental variability by deploying temperature, pH, and DO sensors inside and outside a temperate kelp forest in the Santa Barbara Channel (SBC) throughout the gametogenesis period of a key herbivore, the purple urchin Strongylocentrotus purpuratus. Over the 6 mo period, pH and temperature were slightly elevated inside the kelp forest, accompanied by more predictable, low-frequency variability relative to outside. Adult S. purpuratus were conditioned inside and outside the kelp spanning gametogenesis. The urchins were spawned and their larvae were raised under high (1053 µatm) and low pCO2 (435 µatm) at 15°C in the laboratory to assess their physiological response to the maternal and developmental environments. Larvae raised under high pCO2 were more susceptible to acute thermal stress; however, within each larval treatment, progeny from outside-conditioned mothers had a 0.4°C higher lethal temperature (LT50). Our results indicate that heterogeneity in abiotic factors associated with kelp can have transgenerational effects in the field, and interactions between factors, including temperature and pH, will impact purple urchins as local variability associated with marine heatwaves and upwelling evolves with climate change.