Ocean warming undermines the recovery resilience of New England kelp forests following a fishery-induced trophic cascade.

Ecological theory predicts that kelp forests structured by trophic cascades should experience recovery and persistence of their foundation species when herbivores become rare. Yet, climate change may be altering the outcomes of top-down forcing in kelp forests, especially those located in regions that have rapidly warmed in recent decades, such as the Gulf of Maine. Here, using data collected annually from 30+ sites spanning >350 km of coastline, we explored the dynamics of Maine's kelp forests in the ~20 years after a fishery-induced elimination of sea urchin herbivores. Although forests (Saccharina latissima and Laminaria digitata) had broadly returned to Maine in the late 20th century, we found that forests in northeast Maine have since experienced slow but significant declines in kelp, and forest persistence in the northeast was juxtaposed by a rapid, widespread collapse in the southwest. Forests collapsed in the southwest apparently because ocean warming has-directly and indirectly-made this area inhospitable to kelp. Indeed, when modeling drivers of change using causal techniques from econometrics, we discovered that unusually high summer seawater temperatures the year prior, unusually high spring seawater temperatures, and high sea urchin densities each negatively impacted kelp abundance. Furthermore, the relative power and absolute impact of these drivers varied geographically. Our findings reveal that ocean warming is redefining the outcomes of top-down forcing in this system, whereby herbivore removal no longer predictably leads to a sustained dominance of foundational kelps but instead has led to a waning dominance (northeast) or the rise of a novel phase state defined by "turf" algae (southwest). Such findings indicate that limiting climate change and managing for low herbivore abundances will be essential for preventing further loss of the vast forests that still exist in northeast Maine. They also more broadly highlight that climate change is "rewriting the rules" of nature, and thus that ecological theory and practice must be revised to account for shifting species and processes.

Coral-reef ecology: Expanding urchin disease threatens ecosystem balance.

Sea urchins are critically important herbivores on coral reefs. A new study shows that a disease that decimated sea urchins in the Caribbean in 2022 has spread to the Red Sea, further threatening coral ecosystems.

Mass mortality of diadematoid sea urchins in the Red Sea and Western Indian Ocean.

Sea urchins are primary herbivores on coral reefs, regulating algal biomass and facilitating coral settlement and growth.1,2,3,4,5,6,7,8,9,10,11,12 Recurring mass mortality events (MMEs) of Diadema species Gray, 1825 have been recorded globally,13,14,15,16,17,18,19,20,21,22,23 the most notorious and ecologically significant of which occurred in the Caribbean in 1983,14,17,19,20 contributing to the shift from coral to algal-dominated ecosystems.17,24,25 Recently, first evidence of Diadema setosum mass mortality was reported from the eastern Mediterranean Sea.23 Here, we report extensive mass mortalities of several diadematoid species inhabiting the Red Sea and Western Indian Ocean (WIO)26,27,28 including first evidence of mortalities in the genus Echinothrix Peters, 1853. Mortalities initiated in the Gulf of Aqaba on December 2022 and span the Red Sea, the Gulf of Oman, and the Western Indian Ocean (Réunion Island), with population declines reaching 100% at some sites. Infected individuals are characterized by spine loss and tissue necrosis, resulting in exposed skeletons (i.e., tests) and mortality. Molecular diagnostics of the 18S rRNA gene confirm the presence of a waterborne scuticociliate protozoan most closely related to Philaster apodigitiformis in infected specimens-identical to the pathogen found in the 2022 Caribbean mass mortality of Diadema antillarum.13,15,18 Collapse of these key benthic grazers in the Red Sea and Western Indian Ocean may lead to algal dominance over corals, threatening the stability of coral reefs on a regional scale.29,30,31,32 We issue a warning regarding the further expansion of mortalities and call for immediate monitoring and conservation efforts for these key ecological species.

When species don't move together: Non-concurrent range shifts in Eastern Pacific kelp forest communities.

Species range shifts due to changing ocean conditions are occurring around the world. As species move, they build new interaction networks as they shift from or into new ecological communities. Typically, species ranges are modeled individually, but biotic interactions have been shown to be important to creating more realistic modeling outputs for species. To understand the importance of consumer interactions in Eastern Pacific kelp forest species distributions, we used a Maxent framework to model a key foundation species, giant kelp (Macrocystis pyrifera), and a dominant herbivore, purple sea urchins (Strongylocentrotus purpuratus). With neither species having previously been modeled in the Eastern Pacific, we found evidence for M. pyrifera expansion in the northern section of its range, with no projected contraction at the southern range edge. Despite its known co-occurrence with M. pyrifera, models of S. purpuratus showed a non-concurrent southern range contraction and a co-occurring northern range expansion. While the co-occurring shifts may lead to increased spatial competition for suitable substrate, this non-concurrent contraction could result in community wide impacts such as herbivore release, tropicalization, or ecosystem restructuring.

Effects of macroalgae and sea urchin grazing pressure on zoantharians growth under laboratory conditions.

In the context of ocean warming, thermophilic organisms such as zoantharians are expanding and altering shallow benthic habitats. Here, a four-month laboratory experiment was performed to examine the influence of three types of macroalgae morphotypes common in the Canary Islands (turf algae, Lobophora spp., and crustose coralline algae) on the growth of two zoantharian species, Palythoa caribaeorum and Zoanthus pulchellus. Additionally, the grazing effects of echinoids Diadema africanum and Paracentrotus lividus were assessed as facilitators of substrate colonization by means of controlling macroalgae cover. Colony and algal coverages were measured at the beginning, middle and end of the experiment, and increments were calculated. Results indicated a general decrease in zoantharian colony sizes in contact with different algal types in the absence of sea urchins. However, P. caribaeorum colonies showed significant growth in the presence of D. africanum, highlighting the ecological importance of sea urchins in zoantharian population proliferation and subsequent community modification. This study represents the first investigation into zoantharian-macroalgae interactions under controlled conditions.

Drivers of biological response to fluctuating seawater ph conditions in sea urchin echinus esculentus larvae.

A large body of evidence is documenting the impact of reduced pH on marine species and ecosystems. This information is used to infer the present and future impacts of ocean acidification. However, a vast majority of the studies were performed using constant pH and the high level of pH variability experienced by marine organisms on the coastal zone was often overlooked. Recent studies highlight the key role of this variability in driving biological response to pH as well as species sensitivity to ocean acidification. For example, it was hypothesized that because of local adaptation, the extreme of the present range of pH variability is a good predictor for local biological thresholds. Using a complex experimental design, we investigated what part of the pH variability is driving the biological response of the sea urchin Echinus esculentus larvae. Comparing stable (pH 8.13, 7.82, 7.53) and fluctuating treatments (12 h at pH 8.13 and 12 h at pH 7.53) following natural or inverted diurnal cycles, we were able to show that (i) under constant conditions, low pH deviating from the present range of natural variability had a negative effect on larval growth rate and calcification; (ii) under fluctuating conditions, a desynchronization of the pH variation with the photoperiod led to decreased larval growth rate and calcification; (iii) overall, larval fitness (survival, growth and calcification) was higher under fluctuating conditions as compared to constant. While these data do not support the hypothesis that the minimum pH is the main driver of the biological response, they provide evidence of adaptation to variability in a coastal species with associated a cost of plasticity but not a cost of canalization.

Mesocosm study of PAC-modified clay effects on Karenia brevis cells and toxins, chemical dynamics, and benthic invertebrate physiology.

Modified clay compounds are used globally as a method of controlling harmful algal blooms, and their use is currently under consideration to control Karenia brevis blooms in Florida, USA. In 1400 L mesocosm tanks, chemical dynamics and lethal and sublethal impacts of MC II, a polyaluminum chloride (PAC)-modified kaolinite clay, were evaluated over 72 h on a benthic community representative of Sarasota Bay, which included blue crab (Callinectes sapidus), sea urchin (Lytechinus variegatus), and hard clam (Mercenaria campechiensis). In this experiment, MC II was dosed at 0.2 g L-1 to treat bloom-level densities of K. brevis at 1 × 106 cells L-1. Cell removal in MC II-treated tanks was 57% after 8 h and 95% after 48 h. In the water column, brevetoxin analogs BTx-1 and BTx-2 were found to be significantly higher in untreated tanks at 24 and 48 h, while in MC II-treated tanks, BTx-3 was found to be higher at 48 h and BTx-B5 was found to be higher at 24 and 48 h. In MC II floc, we found no significant differences in BTx-1 or BTx-2 between treatments for any time point, while BTx-3 was found to be significantly higher in the MC II-treated tanks at 48 and 72 h, and BTx-B5 was higher in MC II-treated tanks at 24 and 72 h. Among various chemical dynamics observed, it was notable that dissolved phosphorus was consistently significantly lower in MC II tanks after 2 h, and that turbidity in MC II tanks returned to control levels 48 h after treatment. Dissolved inorganic carbon and total seawater alkalinity were significantly reduced in MC II tanks, and partial pressure of CO2 (pCO2) was significantly higher in the MC II-only treatment after 2 h. In MC II floc, particulate phosphorus was found to be significantly higher in MC II tanks after 24 h. In animals, lethal and sublethal responses to MC II-treated K. brevis did not differ from untreated K. brevis for either of our three species at any time point, suggesting MC II treatment at this dosage has negligible impacts to these species within 72 h of exposure. These results appear promising in terms of the environmental safety of MC II as a potential bloom control option, and we recommend scaling up MC II experiments to field trials in order to gain deeper understanding of MC II performance and dynamics in natural waters.

Transgenerational acclimation to acidified seawater and gene expression patterns in a sea urchin.

Transgenerational responses of susceptible calcifying organisms to progressive ocean acidification are an important issue in reducing uncertainty of future predictions. In this study, a two-generation rearing experiment was conducted using mature Mesocentrotus nudus, a major edible sea urchin that occurs along the coasts of northern Japan. Morphological observations and comprehensive gene expression analysis (RNA-seq) of resulting larvae were performed to examine transgenerational acclimation to acidified seawater. Two generations of rearing experiments showed that larvae derived from parents acclimated to acidified seawater tended to have higher survival and show less reduction in body size when exposed to acidified seawater of the same pH, suggesting that a positive carry-over effect occurred. RNA-seq analysis showed that gene expression patterns of larvae originated from both acclimated and non-acclimated parents to acidified seawater tended to be different than control condition, and the gene expression pattern of larvae originated from acclimated parents was substantially different than that of larvae of non-acclimated and control parents.

Exploring indirect effects of a classic trophic cascade between urchins and kelp on zooplankton and whales.

Kelp forest trophic cascades have been extensively researched, yet indirect effects to the zooplankton prey base and gray whales have not been explored. We investigate the correlative patterns of a trophic cascade between bull kelp and purple sea urchins on gray whales and zooplankton in Oregon, USA. Using generalized additive models (GAMs), we assess (1) temporal dynamics of the four species across 8 years, and (2) possible trophic paths from urchins to kelp, kelp as habitat to zooplankton, and kelp and zooplankton to gray whales. Temporal GAMs revealed an increase in urchin coverage, with simultaneous decline in kelp condition, zooplankton abundance and gray whale foraging time. Trophic path GAMs, which tested for correlations between species, demonstrated that urchins and kelp were negatively correlated, while kelp and zooplankton were positively correlated. Gray whales showed nuanced and site-specific correlations with zooplankton in one site, and positive correlations with kelp condition in both sites. The negative correlation between the kelp-urchin trophic cascade and zooplankton resulted in a reduced prey base for gray whales. This research provides a new perspective on the vital role kelp forests may play across multiple trophic levels and interspecies linkages.

Has the concept of polyspermy prevention been invented in the laboratory?

There is no evidence, nor need, for a fast block to polyspermy in animal oocytes. The idea that oocytes have evolved a mechanism to allow the entry of one spermatozoon and repel all others has, however, gained consensus over the last century. The main culprit is the sea urchin, which has been used for over a century in in vitro studies of the fertilization process. Images of sea urchin oocytes with thousands of sperm attached to the surface are commonplace in textbooks and appeal to the nature of the reader implying an intriguing surface mechanism of sperm selection despite these oocytes being fixed for photography (Figure ). The abundance of gametes in this marine invertebrate and the ease of experimentation have given us the possibility to elucidate many aspects of the mechanism of fertilization, but has also led to ongoing controversies in reproductive biology, one being polyspermy prevention. Kinetic experiments by Rothschild and colleagues in the 1950s led to the hypothesis of a fast partial block to polyspermy in sea urchin oocytes that reduced the probability of a second spermatozoon from entering the oocyte by 1/20th. In the 1970s, Jaffe and colleagues suggested, with circumstantial evidence, that this partial block was due to the sperm-induced depolarization of the oocyte plasma membrane. However, the fate of supernumerary spermatozoa is determined well before the plasma membrane of the oocyte depolarizes. Transmembrane voltage does not serve to regulate sperm entry. Scholastic texts have inadvertently promulgated this concept across the animal kingdom with no logical correlation or experimentation and, as of today, a molecular mechanism to regulate sperm entry in oocytes has not been identified.

Surviving in an Acidifying Ocean: Acid-Base Physiology and Energetics of the Sea Urchin Larva.

The sea urchin larva has been used by biologists for more than a century to study the development and evolution of animals. Surprisingly, very little information has been generated regarding the physiology of this small planktonic organism. However, in the context of anthropogenic CO2-driven ocean acidification (OA), the membrane transport physiology and energetics of this marine model organism have received considerable attention in the past decade. This has led to the discovery of new, exciting physiological systems, including a highly alkaline digestive tract and the calcifying primary mesenchyme cells that generate the larval skeleton. These physiological systems directly relate to the energetics of the organisms when challenged by OA. Here we review the latest membrane transport physiology and energetics in the sea urchin larva, we identify emerging questions, and we point to important future directions in the field of marine physiology in times of rapid climate change.

The behavior of sympatric sea urchin species across an ecosystem state gradient.

Background: In temperate macroalgal forests, sea urchins are considered as a keystone species due to their grazing ability. Given their potential to shape benthic communities, we monitored the habitat use by three sympatric sea urchin species and compared their behaviors in a vegetated habitat (VH) and an adjacent isoyake habitat (IH). Methods: We monitored the environmental conditions and sea urchin density along deep and shallow transects of the VH and IH for over a year. The benthic rugosity at both sites were also surveyed. A mark-recapture experiment was conducted on the two most abundant sea urchins, Diadema setosum and Heliocidaris crassispina, to elucidate sea urchin movement patterns and group dynamics. Results: We found that exposure to waves was highest at the VH while the IH was sheltered. The deep IH experienced the least amount of light due to high turbidity. Water temperature patterns were similar across sites. The VH benthic topography was more rugose compared to the smoother and silt-covered IH substate. Peak macroalgal bloom occurred three months earlier in IH, but macroalgae persisted longer at the shallow VH. Among the sympatric sea urchins, H. crassispina was most abundant at the shallow VH and was observed in pits and crevices. The most abundant across IH and in the deep VH was D. setosum, preferring either crevices or free-living, depending on hydrodynamic conditions. The least abundant species was D. savignyi, and most often observed in crevices. Small and medium sea urchins were most often observed at the IH site, whereas larger sea urchins were more likely observed at the VH. The mark-recapture study showed that D. setosum was found to displace further at the IH, and H. crassispina was more sedentary. Additionally, D. setosum was always observed in groups, whereas H. crassispina was always solitary. Discussion: The behaviors of sympatric urchins, Diadema savignyi, D. setosum and H. crassispina, differed in response to changes in the benthic environment and physical conditions. Sea urchin displacement increased when rugosity and wave action were low. Habitat preference shifted to crevices in seasons with high wave action. In general, the mark-recapture experiment showed that sea urchins displaced further at night.

Acclimation of the Antarctic sea urchin Sterechinus neumayeri to warmer temperatures involves a modulation of cellular machinery.

Global warming is threatening marine Antarctic fauna, which has evolved in isolation in a cold environment for millions of years. Facing increasing temperatures, marine Antarctic invertebrates can either tolerate or develop adaptations to these changes. On a short timescale, their survival and resistance to warming will be driven by the efficiency of their phenotypic plasticity through their capacity for acclimation. The current study aims at evaluating the capacity for acclimation of the Antarctic sea urchin Sterechinus neumayeri to predicted ocean warming scenarios (+2, RCP 2.6 and + 4 °C, RCP 8.5, IPCC et al., 2019) and deciphering the subcellular mechanisms underlying their acclimation. A combination of transcriptomics, physiological (e.g. growth rate, gonad growth, ingestion rate and oxygen consumption), and behavioral-based approaches were used on individuals incubated at 1, 3 and, 5 °C for 22 weeks. Mortality was low at warmer temperatures (20%) and oxygen consumption and ingestion rate seemed to reach a stable state around 16 weeks suggesting that S. neumayeri might be able to acclimate to warmer temperatures (until 5 °C). Transcriptomic analyses highlighted adjustments of the cellular machinery with the activation of replication, recombination, and repair processes as well as cell cycle and division and repression of transcriptional and signal transduction mechanisms and defense processes. These results suggest that acclimation to warmer scenarios might require more than 22 weeks for the Antarctic Sea urchins S. neumayeri but that projections of climate change for the end of the century may not strongly affect the population of S. neumayeri of this part of the Antarctic.

Sunflower sea star predation on urchins can facilitate kelp forest recovery.

The recent collapse of predatory sunflower sea stars (Pycnopodia helianthoides) owing to sea star wasting disease (SSWD) is hypothesized to have contributed to proliferation of sea urchin barrens and losses of kelp forests on the North American west coast. We used experiments and a model to test whether restored Pycnopodia populations may help recover kelp forests through their consumption of nutritionally poor purple sea urchins (Strongylocentrotus purpuratus) typical of barrens. Pycnopodia consumed 0.68 S. purpuratus d-1, and our model and sensitivity analysis shows that the magnitude of recent Pycnopodia declines is consistent with urchin proliferation after modest sea urchin recruitment, and even small Pycnopodia recoveries could generally lead to lower densities of sea urchins that are consistent with kelp-urchin coexistence. Pycnopodia seem unable to chemically distinguish starved from fed urchins and indeed have higher predation rates on starved urchins owing to shorter handling times. These results highlight the importance of Pycnopodia in regulating purple sea urchin populations and maintaining healthy kelp forests through top-down control. The recovery of this important predator to densities commonly found prior to SSWD, whether through natural means or human-assisted reintroductions, may therefore be a key step in kelp forest restoration at ecologically significant scales.

Planktonic Duration of the Bryozoan Cyphonautes Larva and Limits on Growth Rate Imposed by Its Form-Limited Maximum Clearance Rate.

AbstractThe form of the cyphonautes larva of bryozoans changes little during development. The ciliated band that generates the feeding current increases nearly in proportion to body length, so that the maximum rate of clearing planktonic food from a volume of water becomes increasingly low relative to body protein. This development is unlike the other larvae that produce a feeding current with bands of simple cilia. The cyphonautes' growth rate has therefore been predicted to be unusually low when food is scarce. As predicted, cyphonautes larvae of a species of Membranipora starved at concentrations of food that supported growth of pluteus larvae. Comparisons between the cyphonautes and plutei of a sand dollar were for growth from first feeding to metamorphosis, with a mix of two algal species. Another comparison was for growth of cyphonautes at an advanced stage and plutei of a regular sea urchin at an early stage, with food in seawater at a reduced concentration. The low maximum clearance rate did not prevent rapid growth and development of some cyphonautes from egg through metamorphosis when food was abundant. Twenty-nine days for development to metamorphosis in the laboratory with abundant food was close to Yoshioka's estimate of larval duration from the time lag between adult zooid density and larval abundance in a population in the Southern California Bight. Despite individual variation in growth rates and other physiological and environmental influences, simple measures of larval form predicted the differences in larval performance: scarce food extended larval duration for the cyphonautes more than for plutei.

Ocean acidification impacts sperm swimming performance and pHi in the New Zealand sea urchin Evechinus chloroticus.

In sea urchins, spermatozoa are stored in the gonads in hypercapnic conditions (pH<7.0). During spawning, sperm are diluted in seawater of pH>8.0, and there is an alkalinization of the sperm's internal pH (pHi) through the release of CO2 and H+. Previous research has shown that when pHi is above 7.2-7.3, the dynein ATPase flagellar motors are activated, and the sperm become motile. It has been hypothesized that ocean acidification (OA), which decreases the pH of seawater, may have a narcotic effect on sea urchin sperm by impairing the ability to regulate pHi, resulting in decreased motility and swimming speed. Here, we used data collected from the same individuals to test the relationship between pHi and sperm motility/performance in the New Zealand sea urchin Evechinus chloroticus under near-future (2100) and far-future (2150) atmospheric PCO2 conditions (RCP 8.5: pH 7.77, 7.51). Decreasing seawater pH significantly negatively impacted the proportion of motile sperm, and four of the six computer-assisted sperm analysis (CASA) sperm performance measures. In control conditions, sperm had an activated pHi of 7.52. Evechinus chloroticus sperm could not defend pHi in future OA conditions; there was a stepped decrease in the pHi at pH 7.77, with no significant difference in mean pHi between pH 7.77 and 7.51. Paired measurements in the same males showed a positive relationship between pHi and sperm motility, but with a significant difference in the response between males. Differences in motility and sperm performance in OA conditions may impact fertilization success in a future ocean.

Conspecific cues, not starvation, mediate barren urchin response to predation risk.

Prey state and prey density mediate antipredator responses that can shift community structure and alter ecosystem processes. For example, well-nourished prey at low densities (i.e., prey with higher per capita predation risk) should respond strongly to predators. Although prey state and density often co-vary across habitats, it is unclear if prey responses to predator cues are habitat-specific. We used mesocosms to compare the habitat-specific responses of purple sea urchins (Strongylocentrotus purpuratus) to waterborne cues from predatory lobsters (Panulirus interruptus). We predicted that urchins from kelp forests (i.e., in well-nourished condition) tested at low densities typically observed in this habitat would respond more strongly to predation risk than barren urchins (i.e., in less nourished condition) tested at high densities typically observed in this habitat. Indeed, when tested at densities associated with respective habitats, urchins from forests, but not barrens, reduced kelp grazing by 69% when exposed to lobster risk cues. Barren urchins that were unresponsive to predator cues at natural, high densities suddenly responded strongly to lobster cues when conspecific densities were reduced. Strong responses of low densities of barren urchins persisted across feeding history (i.e. 0-64 days of starvation). This suggests that barren urchins can respond to predators but typically do not because of high conspecific densities. Because high densities of urchins in barrens should weaken the non-consumptive effects of lobsters, urchins in these habitats may continue to graze in the presence of predators thereby providing a feedback that maintains urchin barrens.

Reference Genome of the California Sheephead, Semicossyphus pulcher (Labridae, Perciformes), A Keystone Fish Predator in Kelp Forest Ecosystems.

Keystone species are known to play a critical role in kelp forest health, including the well-known killer whales, sea otter, sea urchin, kelp trophic cascade in the Aleutian Islands, Alaska, USA. In California, a major player in the regulation of sea urchin abundance, and in turn, the health of kelp forests ecosystems, is a large wrasse, the California Sheephead, Semicossyphus pulcher. We present a reference genome for this ecologically important species that will serve as a key resource for future conservation research of California's inshore marine environment utilizing genomic tools to address changes in life-history traits, dispersal, range shifts, and ecological interactions among members of the kelp forest ecological assemblages. Our genome assembly of S. pulcher has a total length of 0.794 Gb, which is similar to many other marine fishes. The assembly is largely contiguous (N50 = 31.9 Mb) and nearly complete (BUSCO single-copy core gene content = 98.1%). Within the context of the California Conservation Genomics Project (CCGP), the genome of S. pulcher will be used as an important reference resource for ongoing whole genome resequencing efforts of the species.

Alternations in the foraging behaviour of a primary consumer drive patch transition dynamics in a temperate rocky reef ecosystem.

Understanding the role of animal behaviour in linking individuals to ecosystems is central to advancing knowledge surrounding community structure, stability and transition dynamics. Using 22 years of long-term subtidal monitoring, we show that an abrupt outbreak of purple sea urchins (Strongylocentrotus purpuratus), which occurred in 2014 in southern Monterey Bay, California, USA, was primarily driven by a behavioural shift, not by a demographic response (i.e. survival or recruitment). We then tracked the foraging behaviour of sea urchins for 3 years following the 2014 outbreak and found that behaviour is strongly associated with patch state (forest or barren) transition dynamics. Finally, in 2019, we observed a remarkable recovery of kelp forests at a deep rocky reef. We show that this recovery was associated with sea urchin movement from the deep reef to shallow water. These results demonstrate how changes in grazer behaviour can facilitate patch dynamics and dramatically restructure communities and ecosystems.