Marine heat waves drive bleaching and necrosis of temperate sponges

Bell, James J.; Smith, Robert G.; Micaroni, Valerio; Strano, Francesca; Balemi, Celia A.; Caiger, Paul E.; Miller, Kelsey I.; Spyksma, Arie J. P.; Shears, Nick T.

doi:10.1016/j.cub.2022.11.013

Cited by 23 publications

(19 citation statements)

References 37 publications

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“…Kelp recruitment was observed within control areas, but these were consumed by sea urchins (K. Miller 2022, University of Auckland, personal observation), demonstrating that overgrazing was responsible for the lack of kelp in barrens rather than kelp recruitment failure. Furthermore, similar levels of kelp recovery were observed across the four sites despite varying environmental stressors and disturbance events, such as higher turbidity at Ōtata where kelp display reduced productivity compared to the other sites (Blain et al 2021), or a large marine heatwave across the study region in 2022 (Bell et al 2022). Notably, E. radiata and other macroalgal species are not at the end of their thermal tolerances in this region and not likely to be limited by temperature (Chapman 1966; Wernberg et al 2019 a ; Cornwall et al 2023).…”

Section: Discussionmentioning

confidence: 63%

Large‐scale one‐off sea urchin removal promotes rapid kelp recovery in urchin barrens

Miller,

Balemi,

Bell

et al. 2023

Restoration Ecology

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Sea urchin overgrazing is a leading cause of kelp forest loss and in such cases their removal is increasingly advocated for kelp forest restoration. However, refining removal approaches is needed to improve the efficiency and success of restoration, as most previous removal studies have been small scale and require ongoing removals to maintain low densities and allow kelp recovery. We investigated the effectiveness of one‐off urchin removal from large, semi‐discrete areas of urchin barrens as a tool to promote kelp recovery. We removed sea urchins (Evechinus chloroticus) from four areas (1.6–2 ha) of urchin barrens in northeastern New Zealand. Exposed urchins were reduced to approximately 7% of initial densities and remained low, yet cryptic urchin densities increased after 2 years. Kelp (Ecklonia radiata) and fucoid (Sargassum sinclairii, Carpophyllum spp.) densities increased rapidly in removal areas, but remained constant or declined in adjacent control urchin barren areas. Macroalgal canopy recovery varied among and within removal areas, but increased on average from approximately 5 to 43% in 2 years. Densities of large sea urchin predators did not increase with kelp recovery, likely due to ongoing fishing within removal areas. Our results demonstrate that a single urchin removal from large, semi‐discrete areas of urchin barrens can effectively and efficiently promote rapid multi‐species macroalgal recovery without additional actions (e.g. repeated urchin removals or macroalgae enhancement) for at least 2 years. However, this approach does not restore whole ecosystems and consequently restoration benefits through kelp recovery will be temporary without longer‐term urchin management and/or rebuilding of predator populations.

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Section: Discussionmentioning

confidence: 63%

Large‐scale one‐off sea urchin removal promotes rapid kelp recovery in urchin barrens

Miller,

Balemi,

Bell

et al. 2023

Restoration Ecology

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“…Between 2015 and 2016 a winter marine heatwave was correlated with failed spawning in several marine invertebrates in the Northeastern Pacific [ 65 ]. Considering that tissue regression is known as a morphological response of sponges to extreme temperatures in both experimental and field conditions [ 62 , 66 ], marine heatwaves occurring at the beginning of the reproductive period have the potential to adversely impact early gametogenesis and embryogenesis in sponges by causing the reabsorption of reproductive structures and consequently may disrupt the entire phenological event. It will be important in the future to examine the effects of the MHW timing on phenological events such as gametogenesis and embryogenesis not only in sponges but also in other marine organisms.…”

Section: Discussionmentioning

confidence: 99%

“…Although our knowledge of the physical characteristics of MHWs has rapidly increased over the past decade, the effects of MHWs on biological processes are still not well understood and require particular attention [2]. MHWs have already caused massive coral bleaching events in the tropics [3] and mass mortalities of habitat-forming invertebrates, including sponges and gorgonians, in temperate and polar seas [4][5][6], and the frequency and intensity of MHWs are predicted to increase [7].…”

Section: Introductionmentioning

confidence: 99%

Marine heatwave conditions drive carryover effects in a temperate sponge microbiome and developmental performance

et al. 2023

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Marine heatwaves are increasingly subjecting organisms to unprecedented stressful conditions, but the biological consequences of these events are still poorly understood. Here we experimentally tested the presence of carryover effects of heatwave conditions on the larval microbiome, settlers growth rate and metamorphosis duration of the temperate sponge Crella incrustans . The microbial community of adult sponges changed significantly after ten days at 21°C. There was a relative decrease in symbiotic bacteria, and an increase in stress-associated bacteria. Sponge larvae derived from control sponges were mainly characterised by a few bacterial taxa also abundant in adults, confirming the occurrence of vertical transmission. The microbial community of sponge larvae derived from heatwave-exposed sponges showed significant increase in the endosymbiotic bacteria Rubritalea marina. Settlers derived from heatwave-exposed sponges had a greater growth rate under prolonged heatwave conditions (20 days at 21°C) compared to settlers derived from control sponges exposed to the same conditions. Moreover, settler metamorphosis was significantly delayed at 21°C. These results show, for the first time, the occurrence of heatwave-induced carryover effects across life-stages in sponges and highlight the potential role of selective vertical transmission of microbes in sponge resilience to extreme thermal events.

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“…De Goeij et al (2009) suggested that cell turnover and shedding of choanocytes could be a mechanism used by sponges to prevent permanent damage under environmental stress, and Massaro et al (2012) further hypothesized that thermal stress caused the reduction in choanocyte chamber size and density in Rhopaloeides odorabile exposed to 32 C. In addition, temperatures higher than 31 C increased the expression of heat shock proteins in some species (L opez-Legentil et al 2008;Pantile and Webster 2011;Guzman and Conaco 2016). Although some studies suggested sponges to be more tolerant to ocean warming than other benthic organisms such as corals (Kelmo et al 2013), many studies showed that both acute, short-and long-term exposure to high temperature has caused mass mortality events (e.g., Cebrian et al 2011;Perkins et al 2022;Bell et al 2023). Likely, ocean warming effects on sponges' metabolism are species-specific, and depend on whether a particular species is already near or above its thermal optimum.…”

mentioning

confidence: 99%

“…In addition, temperatures higher than 31°C increased the expression of heat shock proteins in some species (López‐Legentil et al 2008; Pantile and Webster 2011; Guzman and Conaco 2016). Although some studies suggested sponges to be more tolerant to ocean warming than other benthic organisms such as corals (Kelmo et al 2013), many studies showed that both acute, short‐ and long‐term exposure to high temperature has caused mass mortality events (e.g., Cebrian et al 2011; Perkins et al 2022; Bell et al 2023). Likely, ocean warming effects on sponges' metabolism are species‐specific, and depend on whether a particular species is already near or above its thermal optimum.…”

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confidence: 99%

Warm‐adapted sponges resist thermal stress by reallocating carbon and nitrogen resources from cell turnover to somatic growth

Maggioni,

Raimbault,

Chateau

et al. 2024

Limnology & Oceanography

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Ocean warming will affect the functioning of coral reef ecosystems with unknown cascading effects. Any perturbation in the ability of sponges to recycle the dissolved organic matter released by primary producers and make it available to higher trophic levels, might have unknown consequences for the reef trophic chain. Biogeochemical processes were measured in the sponge Rhabdastrella globostellata from the semi‐enclosed lagoon of Bouraké, where temperatures reach 33.8°C and fluctuates by 6.5°C on a daily basis, and from a control reef (28°C). Using 13C‐ and 15N‐labeled coral mucus, we experimentally investigated to what extent high temperature affected the carbon (C) and nitrogen (N) resources allocation in the sponge tissue and detritus. Sponges from Bouraké maintained at 32°C incorporated more 13C‐ and 15N‐labeled coral mucus in the tissue and showed less detritus release when compared with sponges maintained at 28°C. In contrast, at 32°C control sponges showed lower 13C‐ and 15N‐labeled coral mucus incorporation in tissue and higher release of detritus. Our results suggest that sponges adapted to extreme temperatures of Bouraké were able to reallocate C and N resources from cell turnover to somatic growth and reduce tissue damage. In contrast, non‐adapted sponges at the control reef lack this mechanism and underwent tissue disintegration, highlighting the lethal effect of future warming. The change in C and N allocation in adapted sponges suggests a potential adaptation mechanism that allows R. globostellata to survive under thermal stress, but it could alter the availability of essential sources of energy with unknown consequences on the future reef trophic interactions.

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Marine heat waves drive bleaching and necrosis of temperate sponges

Cited by 23 publications

References 37 publications

Large‐scale one‐off sea urchin removal promotes rapid kelp recovery in urchin barrens

Large‐scale one‐off sea urchin removal promotes rapid kelp recovery in urchin barrens

Marine heatwave conditions drive carryover effects in a temperate sponge microbiome and developmental performance

Warm‐adapted sponges resist thermal stress by reallocating carbon and nitrogen resources from cell turnover to somatic growth

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