A Limpet’s Legacy: Carry-Over Effects across Life Stages and Generations Caused by Global Change Stressors
Global change is increasingly impacting coastal marine systems. Organisms inhabiting the intertidal zone may be especially vulnerable to additional anthropogenic influences, which augment the naturally stressful, highly variable conditions to which they are already subjected and may lead to the manifestation of artificially severe carry-over effects (COEs). In marine invertebrates with complex life histories, COEs can occur between life stages, when the conditions experienced by one stage influence the characteristics or performance of the next, as well as trans-generationally, in which case the environment experienced by a parental generation affects offspring. Most of the existing literature surrounding COEs focuses only on those between life stages or generations, seldom both simultaneously, and do so with the implementation of only a single stressor. In nature however, organisms may be affected by both forms of COE, since the presence of one does not preclude the other, and are invariably subjected to multiple co-occurring stressors that can interact in complex ways. Consequently, how trans-generational COEs might impact the propagation of stress through offspring life stages remains unclear, and how these processes operate in a global change context is little understood. It was here aimed to elucidate the role of COEs under ongoing global change by addressing these common literature imitations and taking the novel approach of examining how the effects of multiple, global change-associated stressors carry-over from a parental generation through their offspring’s life stages in order to provide a more realistic representation of the conditions under which COEs manifest in the field. This was done using Siphonaria australis, an intertidal pulmonate limpet that deposits benthic egg masses, from which hatch planktonic veliger larvae. Adult S. australis were subjected to one of four treatments for 4h/day over four weeks to induce trans-generational COEs: a no-stress control, a pollution treatment with added copper (5.0μg/L), a “climate change” treatment with elevated temperature (25°C) and UVR (1.7W/m2), and a full global change treatment incorporating all three stressors. At the end of this period, the egg masses laid under each of these adult treatments were subjected to further experimentation for two weeks by being redistributed among the same four treatments again, so as to produce 16 unique treatment histories of adult-to-egg mass stress. Of these, 11 provided successfully hatching larvae, which were reared and observed for COEs between life stages (from egg to larva) under ambient conditions (ie. no added stressors) for 27 days. In adult S. australis survivor size, the size of egg masses laid and the size of individual eggs varied in complex ways over time and across treatments, while the number of survivors was unaffected by stress. Egg masses were unaffected in terms of hatching time but displayed strong responses to parental and developmental stress exposure through hatching success, and the percentage of viable eggs per egg mass, with the latter clearly declining according to adult treatment severity and both showing trans-generational COEs. Larval characteristics were extremely varied across treatment histories and highly context-dependent as hatching size, size reached by 27 days, growth rate, and size at death all showed evidence of COEs between generations and life stages, as well as interaction between both types of COE, with the number of survivors again being the only unaffected response variable. Overall, trans-generational COEs were slightly more common than those between life stages. These results show that both forms of COE, each triggered by exposure to multiple stressors in progenitors and developmental stages, interact to form highly context-dependent legacies of mostly impaired performance in S. australis larvae. This implies that COEs may become more prominent with worsening stressors in the future and suggests that the role of COEs in the persistence of marine invertebrates under ongoing global change may so far have been underestimated by the existing literature.