The impact of marine heatwaves on rocky intertidal communities: evidence of accumulative carryover effects of marine heatwaves

Abstract

The frequency and duration of marine heat waves (MHWs) have recently increased. There is therefore an urgent need to understand the response of marine organisms to MHWs. However, most estimates of MHW impacts on abundances include the effects of environmental stochasticity other than the MHWs. In addition, although MHWs sometimes persist for year-round or occur repeatedly for shorter periods, the accumulative carryover effects (ACEs)— the effects of sequential events accumulating additively over time— of MHWs on organisms have never been evaluated. Furthermore, the relationship between species niche traits other than thermal niches and susceptibility to MHWs is unknown. We examined the impacts of MHWs in southeastern Hokkaido, northern Japan, in summer from 2010 to 2016 on rocky intertidal communities by distinguishing MHW effects from environmental stochasticity. We asked (1) Did MHWs have ACEs on four major functional groups: macroalgae, sessile invertebrates, herbivorous invertebrates, and carnivorous invertebrates? (2) Does ignoring ACEs lead to biased assessments? (3) How did the effects of the MHWs on functional groups and their subsequent recovery differ? And (4) How does the susceptibility to MHWs differ with species niche (thermal and vertical) traits? We detected ACEs of MHWs and found that if they are ignored, the effects of MHWs can be underestimated. Although MHWs are known to reduce the abundance of macroalgae and increase that of sessile invertebrates in rocky intertidal habitats, our results show that macroalgal abundance increased during and after MHWs, whereas sessile invertebrates showed no change during or after MHWs. The abundance of herbivorous mollusks decreased during and after MHWs. Carnivorous invertebrates declined during MHWs and in the first year after MHWs. During and after MHWs, abundances of species with low thermal niches decreased and those with high thermal niches increased. There were no differences in response to MHWs between vertical niches when accumulative carryover effects were ignored. These results emphasize the importance of considering ACEs when assessing the response of marine organisms to MHWs, and that more studies of these responses are needed for a variety of ecosystems, regions and organisms to predict the responses of marine organisms.

A Case for Trans-Regional Intertidal Research in Unstudied Areas in the Northeast and Southeast Pacific: Filling the Gaps

“…Blanchette et al [30] have discovered patterns of diversity on a broad regional scale from southeast Alaska to southern California, with seven distinct biogeographical groups defined based on patterns in similarity. In the Southeast Pacific, Ibanez et al [11] and Valqui et al [10] have accomplished similar work by identifying localized patterns, shifts in biological compositions, and a shifting zone of transition following disturbance from El Niño in Peru between 4 • S and 14 • S. Each work concludes with a statement of need to carry forward census efforts on large-and small-region scales in unstudied or poorly studied areas in order to collect the necessary biogeographic data on contiguous and temporal scales [8,10,11,26,85]. Mussels (family Mytilidae) are a foundation species found throughout the intertidal zone and have increasingly become the subject of research due to their abundance worldwide, which positions them as a sentinel species for measuring the physiological responses and rates of mortality from environmental stress and human disturbance [1,[87][88][89][90][91].…”

“…Today, much of the intertidal research in the eastern and western Pacific has occurred along semi-continuous coastlines or a patchwork of latitudes with a focus on characterizing localscale species diversity and abundance, spatial turnover, hierarchical structure, range shifts, and the relationship between biological and oceanographic processes [1,8,11,13,19,83,84]. In the western Pacific, Okuda et al [13] have discerned regional-scale gradients in richness and beta (turnover) diversity, and more recently, small-scale accumulative carryover effects have been identified among functional and trophic groups during and after chronic marine heatwaves in Hokkaido [85]. In the central north Pacific, Konar et al [86] have identified depth-stratified differences in taxonomic hierarchies, invertebrate abundance and macro-algal biomass in intertidal and subtidal communities in Kodiak, Kachemak Bay, and Prince William Sound.…”

“…In the South Pacific, the "Coastal El Niño" marine heatwave manifested in the austral summer of 2017, resulting in range shifts and changes in abundance of intertidal taxa on local scales [10] as well as shifts in the functional group structure and species composition of intertidal mussel communities along the coast of Peru [120]. As marine heatwaves become more frequent, the question becomes one of predicting cumulative carryover effects identified by Ishida et al [85] and changes in algal biomass and patterns of growth, particularly in the intertidal communities of Southeast Alaska as the climate continues to warm [121] (Figure 2). The relevancy of predicting carryover effects in intertidal systems in poorly studied or unstudied regions is attributed to the potential for these systems to become significantly altered by localized and regional shifts in trophic and functional groups, as well as alterations in the services provided by decreased algal biomass.…”

Immediate impact of the 2021 harmful algal bloom in southeast Hokkaido on the rocky intertidal community and its spatial variation

“…While various year-to-year environmental fluctuations may drive community dynamics in rocky intertidal assemblages (Thompson et al ., 2002; Menge et al ., 2003; Ishida et al ., 2023), their influences on the results of this study should be small. From October 2020 to October 2021, there was no other disturbance that would cause massive mortality (e.g., earthquake, tsunami, typhoon, ice scouring, marine heatwave, etc.)…”

“…To evaluate the effects of HAB on each species ( i ) at the regional scale ( ES REGION,i ) and each functional group ( j ) at each shore ( k ) ( ES SHORE,j,k ), we calculated the effect sizes ( ES ) of the abundance ( A ) from the pre-HAB period (2004–2020) to the post-HAB period (2021) with the following formulas (Iwasaki et al ., 2016; Noda et al ., 2017; Iwasaki & Noda, 2017; Ishida et al ., 2023): where log ( A REGION,i,post − HAB ) represents the log 10 (abundance) of each species in the post-HAB year, log ( Ā REGION,i,pre−HAB ) and SD ( log ( A REGION,i,pre−HAB )) represent the mean and standard deviation of the log 10 (abundance) of each species during the pre-HAB period, respectively; log ( A REGION,j,k,post − HAB + 0.5) represents the log 10 (abundance + 0.5) of each functional group at each shore in the post-HAB year, log ( Ā REGION,j,k,pre − HAB + 0.5) and SD log ( A REGION,j,k,pre − HAB + 0.5) represent the mean and standard deviation of log 10 (abundance + 0.5) of each functional group at each shore during the pre-HAB period, respectively. An effect size greater than 1.96 in absolute value suggests that the abundance in the post-HAB year changed significantly compared with the pre-HAB period.…”