Sponge functional roles in a changing world.

Sponges are ecologically important benthic organisms with many important functional roles. However, despite increasing global interest in the functions that sponges perform, there has been limited focus on how such functions will be impacted by different anthropogenic stressors. In this review, we describe the progress that has been made in our understanding of the functional roles of sponges over the last 15 years and consider the impacts of anthropogenic stressors on these roles. We split sponge functional roles into interactions with the water column and associations with other organisms. We found evidence for an increasing focus on functional roles among sponge-focused research articles, with our understanding of sponge-mediated nutrient cycling increasing substantially in recent years. From the information available, many anthropogenic stressors have the potential to negatively impact sponge pumping, and therefore have the potential to cause ecosystem level impacts. While our understanding of the importance of sponges has increased in the last 15 years, much more experimental work is required to fully understand how sponges will contribute to reef ecosystem function in future changing oceans.

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

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.

Marine heat waves drive bleaching and necrosis of temperate sponges.

Marine heat waves (MHWs) are extended periods of excessively warm water1 that are increasing in frequency, duration, intensity, and impact, and they likely represent a greater threat to marine ecosystems than the more gradual increases in sea surface temperature.2,3,4 Sponges are major and important components of global benthic marine communities,5,6,7 with earlier studies identifying tropical sponges as potential climate change "winners."8,9,10,11 In contrast, cold-water sponges may be less tolerant to predicted ocean warming and concurrent MHWs. Here, we report how a series of unprecedented MHWs in New Zealand have impacted millions of sponges at a spatial scale far greater than previously reported anywhere in the world. We reported sponge tissue necrosis12 and bleaching (symbiont loss/dysfunction),13 which have been previously associated with temperature stress,6,12,14 for three common sponge species across multiple biogeographical regions, with the severity of impact being correlated with MHW intensity. Given the ecological importance of sponges,15 their loss from these rocky temperate reefs will likely have important ecosystem-level consequences.

Global status, impacts, and management of rocky temperate mesophotic ecosystems.

The ecology and function of rocky temperate mesophotic ecosystems (TMEs) remain poorly understood globally despite their widespread distribution. They typically occur at 20-150 m (the limit of photosynthesis), and on rocky substratum they support rich benthic communities and mobile fauna. We determined the distribution of rocky TMEs, their conservation status, and their most characteristic biological groups. Rocky TMEs were dominated by algae, turf-invertebrate matrices (<50 m only), sponges, bryozoans, and cnidarians. The community composition of TMEs differed significantly from shallow (0-15 m) subtidal reefs. Data were geographically biased and variable, available only from the North and South Atlantic, Mediterranean, and Temperate Australasia. Degree of protection of rocky TMEs varied considerably across the world. The biggest threats to rocky TMEs were identified changes in temperature, sedimentation rates, nutrient concentrations, and certain fishing types. We propose a conservation framework to inform future rocky TME management and conservation, highlighting the need to recognize the importance of these biologically diverse and functionally important ecosystems.

Resumen La ecología y la función de los ecosistemas mesofóticos templados (TME) rocosos todavía no están muy comprendidas a nivel mundial a pesar de su amplia distribución. Comúnmente se encuentran entre los 20 y los 150 metros (el límite de la fotosíntesis) sobre sustratos rocosos que mantienen comunidades bénticas diversas y fauna móvil. Determinamos la distribución, estado de conservación y grupos biológicos más característicos de los TME rocosos. Estos ecosistemas estuvieron dominados por algas, matrices de invertebrados de pastos marinos (solamente a <50 m), esponjas marinas, briozoos y cnidarios. La composición comunitaria de los TME difirió significativamente de los arrecifes submareales someros (0-15 m). Los datos estuvieron sesgados geográficamente y fueron variables, pues sólo estaban disponibles para el Atlántico norte y sur, el Mediterráneo y la Australasia templada. El nivel de protección de los TME rocosos varió considerablemente en todo el mundo. Las principales amenazas que enfrenta este ecosistema son los cambios en la temperatura, las tasas de sedimentación, la concentración de nutrientes y ciertos tipos de pesca. Proponemos un encuadre de conservación para orientar a futuro la gestión y conservación de los TME, el cual destaque la necesidad de reconocer la importancia de estos ecosistemas biológicamente diversos y funcionalmente importantes.

Near-future extreme temperatures affect physiology, morphology and recruitment of the temperate sponge Crella incrustans.

Current rates of greenhouse gas emissions are leading to a rapid increase in global temperatures and a greater occurrence of extreme climatic events such as marine heatwaves. In this study, we assessed the effects of thermal conditions predicted to occur within the next 40 years (SSP3-7.0 scenario of IPCC, 2021) on the respiration rate, buoyant weight, morphology and recruitment of the temperate model sponge Crella incrustans. Under predicted average temperatures (+ 2.5 °C, over the local mean), C. incrustans did not show any physiological and morphological changes compared to current conditions. However, when exposed to a simulated marine heatwave (16 days duration and a thermal peak at 22 °C), there was a large increase in sponge respiration rate, significant weight loss resulting from tissue regression, and sponge mortality. The simulated marine heatwave resulted also in a shorter period of recruitment, lower recruitment rate and higher mortality of settlers. Despite the tissue regression, the majority of sponges that survived the extreme temperatures showed respiration rates similar to controls 13 days after the thermal peak, indicating some resilience of C. incrustans to extreme thermal events. Our study shows that marine heatwaves will significantly impact the physiology, morphology, and recruitment of temperate sponges under near-future conditions, but that these sponges are likely to persist in warmer oceans.

Adaptive strategies of sponges to deoxygenated oceans.

Ocean deoxygenation is one of the major consequences of climate change. In coastal waters, this process can be exacerbated by eutrophication, which is contributing to an alarming increase in the so-called 'dead zones' globally. Despite its severity, the effect of reduced dissolved oxygen has only been studied for a very limited number of organisms, compared to other climate change impacts such as ocean acidification and warming. Here, we experimentally assessed the response of sponges to moderate and severe simulated hypoxic events. We ran three laboratory experiments on four species from two different temperate oceans (NE Atlantic and SW Pacific). Sponges were exposed to a total of five hypoxic treatments, with increasing severity (3.3, 1.6, 0.5, 0.4 and 0.13 mg O2  L-1 , over 7-12-days). We found that sponges are generally very tolerant of hypoxia. All the sponges survived in the experimental conditions, except Polymastia crocea, which showed significant mortality at the lowest oxygen concentration (0.13 mg O2  L-1 , lethal median time: 286 h). In all species except Suberites carnosus, hypoxic conditions do not significantly affect respiration rate down to 0.4 mg O2  L-1 , showing that sponges can uptake oxygen at very low concentrations in the surrounding environment. Importantly, sponges displayed species-specific phenotypic modifications in response to the hypoxic treatments, including physiological, morphological and behavioural changes. This phenotypic plasticity likely represents an adaptive strategy to live in reduced or low oxygen water. Our results also show that a single sponge species (i.e., Suberites australiensis) can display different strategies at different oxygen concentrations. Compared to other sessile organisms, sponges generally showed higher tolerance to hypoxia, suggesting that sponges could be favoured and survive in future deoxygenated oceans.

Regime shifts on tropical coral reef ecosystems: future trajectories to animal-dominated states in response to anthropogenic stressors.

Despite the global focus on the occurrence of regime shifts on shallow-water tropical coral reefs over the last two decades, most of this research continues to focus on changes to algal-dominated states. Here, we review recent reports (in approximately the last decade) of regime shifts to states dominated by animal groups other than zooxanthellate Scleractinian corals. We found that while there have been new reports of regime shifts to reefs dominated by Ascidacea, Porifera, Octocorallia, Zoantharia, Actiniaria and azooxanthellate Scleractinian corals, some of these changes occurred many decades ago, but have only just been reported in the literature. In most cases, these reports are over small to medium spatial scales (<4 × 104 m2 and 4 × 104 to 2 × 106 m2, respectively). Importantly, from the few studies where we were able to collect information on the persistence of the regime shifts, we determined that these non-scleractinian states are generally unstable, with further changes since the original regime shift. However, these changes were not generally back to coral dominance. While there has been some research to understand how sponge- and octocoral-dominated systems may function, there is still limited information on what ecosystem services have been disrupted or lost as a result of these shifts. Given that many coral reefs across the world are on the edge of tipping points due to increasing anthropogenic stress, we urgently need to understand the consequences of non-algal coral reef regime shifts.

Vulnerability of Temperate Mesophotic Ecosystems (TMEs) to environmental impacts: Rapid ecosystem changes at Lough Hyne Marine Nature Reserve, Ireland.

Temperate Mesophotic Ecosystems (TMEs) are stable habitats, usually dominated by slow-growing, long-lived sessile invertebrates and sciaphilous algae. Organisms inhabiting TMEs can form complex three-dimensional structures and support many commercially important species. However, TMEs have been poorly studied, with little known about their vulnerability to environmental impacts. Lough Hyne Marine Nature Reserve (Ireland) supports TMEs in shallower waters (12-40 m) compared with other locations (30-150+ m) as a result of the unusual hydrodynamic conditions. Here, we report changes that have occurred on the sponge-dominated cliffs at Lough Hyne between 1990 and 2019, providing insights into TME long-term stability and vulnerability to environmental impacts. Our main finding was a marked decline in most three-dimensional sponges at the internal sites of the lough. This was likely the result of one or more mass mortality events that occurred between 2010 and 2015. We also found an increase in ascidians, which might have been more tolerant and benefited from the space freed by the sponge mortality. Finally, in the most recent surveys, we found a high abundance of sponge recruits, indicating that a natural recovery may be underway. The possible factors involved in these community changes include eutrophication, increased temperature, and a toxic event due to an anomaly in the oxycline breakdown. However, the absence of comprehensive monitoring of biotic and abiotic variables makes it impossible to identify the cause with certainty. Our Lough Hyne example shows the potential vulnerability of TMEs to short-term disturbance events, highlighting the importance of monitoring these habitats globally to ensure they are appropriately conserved.

Interocean patterns in shallow water sponge assemblage structure and function.

Sponges are a major component of benthic ecosystems across the world and fulfil a number of important functional roles. However, despite their importance, there have been few attempts to compare sponge assemblage structure and ecological functions across large spatial scales. In this review, we examine commonalities and differences between shallow water (<100 m) sponges at bioregional (15 bioregions) and macroregional (tropical, Mediterranean, temperate, and polar) scales, to provide a more comprehensive understanding of sponge ecology. Patterns of sponge abundance (based on density and area occupied) were highly variable, with an average benthic cover between ~1 and 30%. Sponges were generally found to occupy more space (percentage cover) in the Mediterranean and polar macroregions, compared to temperate and tropical macroregions, although sponge densities (sponges m-2 ) were highest in temperate bioregions. Mean species richness standardised by sampling area was similar across all bioregions, except for a few locations that supported very high small-scale biodiversity concentrations. Encrusting growth forms were generally the dominant sponge morphology, with the exception of the Tropical West Atlantic, where upright forms dominated. Annelids and Arthropods were the most commonly reported macrofauna associated with sponges across bioregions. With respect to reproduction, there were no patterns in gametic development (hermaphroditism versus gonochorism), although temperate, tropical, and polar macroregions had an increasingly higher percentage of viviparous species, respectively, with viviparity being the sole gamete development mechanism reported for polar sponges to date. Seasonal reproductive timing was the most common in all bioregions, but continuous timing was more common in the Mediterranean and tropical bioregions compared to polar and temperate bioregions. We found little variation across bioregions in larval size, and the dominant larval type across the globe was parenchymella. No pattens among bioregions were found in the limited information available for standardised respiration and pumping rates. Many organisms were found to predate sponges, with the abundance of sponge predators being higher in tropical systems. While there is some evidence to support a higher overall proportion of phototrophic species in the Tropical Austalian bioregion compared to the Western Atlantic, both also have large numbers of heterotrophic species. Sponges are important spatial competitors across all bioregions, most commonly being reported to interact with anthozoans and algae. Even though the available information was limited for many bioregions, our analyses demonstrate some differences in sponge traits and functions among bioregions, and among macroregions. However, we also identified similarities in sponge assemblage structure and function at global scales, likely reflecting a combination of regional- and local-scale biological and physical processes affecting sponge assemblages, along with common ancestry. Finally, we used our analyses to highlight geographic bias in past sponge research, and identify gaps in our understanding of sponge ecology globally. By so doing, we identified key areas for future research on sponge ecology. We hope that our study will help sponge researchers to consider bioregion-specific features of sponge assemblages and key sponge-mediated ecological processes from a global perspective.