Survivors of Climate Driven Abalone Mass Mortality Exhibit Declines in Health and Reproduction Following Kelp Forest Collapse

Marine ecosystems are vulnerable to climate driven events such as marine heatwaves yet we have a poor understanding of whether they will collapse or recover. Kelp forests are known to be susceptible, and there has been a rise in sea urchin barrens around the world. When temperatures increase so do physiological demands while food resources decline, tightening metabolic constraints. In this case study, we examine red abalone (Haliotis rufescens) looking at sublethal impacts and their prospects for recovery within kelp forests that have shifted to sea urchin barrens. Abalone are a recreationally fished species that once thrived in northern California’s bull kelp forests but have recently suffered mass mortalities since the 2014–2016 marine heatwave. Quantitative data exist on the health and reproduction of abalone both prior to and after the collapse. The survivors of the mass mortality show a 2-year lag in body and gonad condition indices. After the lag, body and gonad indexes decreased substantially, as did the relationship between shell length and body weight. Production of mature eggs per female declined by 99% (p < 0.001), and the number of eggs per gram of female body weight (2,984/g) declined to near zero (9/g). The number of males with sperm was reduced by 33%, and the sperm abundance score was reduced by 28% (p = 0.414). We observed that these reductions were for mature eggs and sperm while immature eggs and spermatids were still present in large numbers. In the lab, after reintroduction of kelp, weight gains were quickly lost following a second starvation period. This example illustrates how climate-driven declines in foundation species can suppress recovery of the system by impacting body condition and future reproduction of surviving individuals. Given the poor reproductive potential of the remaining abalone in northern California, coupled with ongoing mortality and low kelp abundances, we discuss the need to maintain the fishing moratorium and implement active abalone restoration measures. For fished species, such as abalone, this additional hurdle to recovery imposed by changes in climate is critical to understand and incorporate into resource management and restoration.

Effect of a cold event on population and community of pit-inhabiting sea urchins in Western Pacific coasts

Coastal tide pools in southern Japan are inhabited by the rock-boring sea urchin Echinostrephus molaris, which excavate pits in the substrate. These pits are subsequently used by non-boring sea urchins such as Anthocidaris crassispina and Echinometra sp. B, and the recolonized pits are often inhabited by a commensal limpet-like trochid snail species, Broderipia iridescens. We explored the population and community dynamics of these sea urchins and the limpet-like snail by monitoring occupancy of 512 pits in tide pools in Shirahama, Japan from May 2017–May 2019. Initially, nearly all pits were occupied by any one of the three sea urchin species, but an unusual cold event in February 2018 caused a mass die off of these sea urchins. After this event, occupancy decreased from 99% to 15%, and the tropical species Echinometra sp. B disappeared from the study pools. We observed slow population recovery of E. molaris and A. crassispina, provably via migration of sub-adults from the subtidal zone. Turnover rate of the pit-occupying sea urchin species was <1.0% before the cold event, but drastically increased after the cold event. Population size of the commensal snail decreased along with those of their host, but the rate of commensalism was constant at 50–55% throughout the study period, suggesting that these snails followed their host sea urchins repeating inter-pit migration. Despite mass mortality and slow recovery, the sea urchin density remained high enough to maintain persistent sea urchin barrens throughout the study period.

Trophic downgrading reduces spatial variability on rocky reefs

Trophic downgrading in coastal waters has occurred globally during recent decades. On temperate rocky reefs, this has resulted in widespread kelp deforestation and the formation of sea urchin barrens. We hypothesize that the intact kelp forest communities are more spatially variable than the downgraded urchin barren communities, and that these differences are greatest at small spatial scales where the influence of competitive and trophic interactions is strongest. To address this, benthic community surveys were done in kelp forests and urchin barrens at nine islands spanning 1230 km of the Aleutian Archipelago where the loss of predatory sea otters has resulted in the trophic downgrading of the region’s kelp forests. We found more species and greater total spatial variation in community composition within the kelp forests than in the urchin barrens. Further, the kelp forest communities were most variable at small spatial scales (within each forest) and least variable at large spatial scales (among forests on different islands), while the urchin barren communities followed the opposite pattern. This trend was consistent for different trophic guilds (primary producers, grazers, filter feeders, predators). Together, this suggests that Aleutian kelp forests create variable habitats within their boundaries, but that the communities within these forests are generally similar across the archipelago. In contrast, urchin barrens exhibit relatively low variability within their boundaries, but these communities vary substantially among different barrens across the archipelago. We propose this represents a shift from small-scale biological control to large-scale oceanographic control of these communities.

Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens

Extreme climatic events have recently impacted marine ecosystems around the world, including foundation species such as corals and kelps. Here, we describe the rapid climate-driven catastrophic shift in 2014 from a previously robust kelp forest to unproductive large scale urchin barrens in northern California. Bull kelp canopy was reduced by >90% along more than 350 km of coastline. Twenty years of kelp ecosystem surveys reveal the timing and magnitude of events, including mass mortalities of sea stars (2013-), intense ocean warming (2014–2017), and sea urchin barrens (2015-). Multiple stressors led to the unprecedented and long-lasting decline of the kelp forest. Kelp deforestation triggered mass (80%) abalone mortality (2017) resulting in the closure in 2018 of the recreational abalone fishery worth an estimated $44 M and the collapse of the north coast commercial red sea urchin fishery (2015-) worth $3 M. Key questions remain such as the relative roles of ocean warming and sea star disease in the massive purple sea urchin population increase. Science and policy will need to partner to better understand drivers, build climate-resilient fisheries and kelp forest recovery strategies in order to restore essential kelp forest ecosystem services.