Dataset Information

Population collapse of habitat-forming species in the Mediterranean: a long-term study of gorgonian populations affected by recurrent marine heatwaves.

ABSTRACT: Understanding the resilience of temperate reefs to climate change requires exploring the recovery capacity of their habitat-forming species from recurrent marine heatwaves (MHWs). Here, we show that, in a Mediterranean highly enforced marine protected area established more than 40 years ago, habitat-forming octocoral populations that were first affected by a severe MHW in 2003 have not recovered after 15 years. Contrarily, they have followed collapse trajectories that have brought them to the brink of local ecological extinction. Since 2003, impacted populations of the red gorgonian Paramuricea clavata (Risso, 1826) and the red coral Corallium rubrum (Linnaeus, 1758) have followed different trends in terms of size structure, but a similar progressive reduction in density and biomass. Concurrently, recurrent MHWs were observed in the area during the 2003-2018 study period, which may have hindered populations recovery. The studied octocorals play a unique habitat-forming role in the coralligenous assemblages (i.e. reefs endemic to the Mediterranean Sea home to approximately 10% of its species). Therefore, our results underpin the great risk that recurrent MHWs pose for the long-term integrity and functioning of these emblematic temperate reefs.

SUBMITTER: Gomez-Gras D

PROVIDER: S-EPMC8692971 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Population collapse of habitat-forming species in the Mediterranean: a long-term study of gorgonian populations affected by recurrent marine heatwaves.

Gómez-Gras D D Linares C C López-Sanz A A Amate R R Ledoux J B JB Bensoussan N N Drap P P Bianchimani O O Marschal C C Torrents O O Zuberer F F Cebrian E E Teixidó N N Zabala M M Kipson S S Kersting D K DK Montero-Serra I I Pagès-Escolà M M Medrano A A Frleta-Valić M M Dimarchopoulou D D López-Sendino P P Garrabou J J

Proceedings. Biological sciences 20211222 1965

Understanding the resilience of temperate reefs to climate change requires exploring the recovery capacity of their habitat-forming species from recurrent marine heatwaves (MHWs). Here, we show that, in a Mediterranean highly enforced marine protected area established more than 40 years ago, habitat-forming octocoral populations that were first affected by a severe MHW in 2003 have not recovered after 15 years. Contrarily, they have followed collapse trajectories that have brought them to the br ...[more]

PMID: 34933599

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Project description:Extreme climatic events (ECEs), such as marine heatwaves (MHWs), are a major threat to biodiversity. Understanding the variability in ecological responses to recurrent ECEs within species and underlying drivers arise as a key issue owing to their implications for conservation and population recovery. Yet, our knowledge on such ecological responses is limited since it has been frequently gathered following "single-event approaches" focused on one particular event. These approaches provide snapshots of ecological responses but fall short of capturing heterogeneity patterns that may occur among recurrent ECEs, questioning current predictions regarding biodiversity trends. Here, we adopt a "multiple events" perspective to characterize the effects of recurrent ECEs on the ecological responses in Paramuricea clavata, a Mediterranean temperate coral threatened by MHWs. Through a common-garden experiment repeated three consecutive years with the same individuals from three populations, we assessed the respective roles of environmental (year effect), genetic (population effect), and phenotypic (population-by-environment interactions effect) components in the ecological response to recurrent heat stress. The environmental component (year) was the main driver underlying the responses of P. clavata colonies across experiments. To build on this result, we showed that: (i) the ecological responses were not related to population (genetic isolation) and individual (multilocus heterozygosity) genetic make-up, (ii) while all the individuals were characterized by a high environmental sensitivity (genotype-by-environment interactions) likely driven by in situ summer thermal regime. We confront our experimental results to in situ monitoring of the same individuals conducted in 2022 following two MHWs (2018, 2022). This confirms that the targeted populations harbor limited adaptive and plastic capacities to on-going recurrent ECEs and that P. clavata might face unavoidable population collapses in shallow Mediterranean waters. Overall, we underscore the need to consider the recurrence of ECEs to assess threats to biodiversity and to forecast its evolution.

Project description:BackgroundIn the ocean, the variability of environmental conditions found along depth gradients exposes populations to contrasting levels of perturbation, which can be reflected in the overall patterns of species genetic diversity. At shallow sites, resource availability may structure large, persistent and well-connected populations with higher levels of diversity. In contrast, the more extreme conditions, such as thermal stress during heat waves, can lead to population bottlenecks and genetic erosion, inverting the natural expectation. Here we examine how genetic diversity varies along depth for a long-lived, important ecosystem-structuring species, the red gorgonian, Paramuricea clavata.MethodsWe used five polymorphic microsatellite markers to infer differences in genetic diversity and differentiation, and to detect bottleneck signs between shallow and deeper populations across the Atlantic Ocean and the Mediterranean Sea. We further explored the potential relationship between depth and environmental gradients (temperature, ocean currents, productivity and slope) on the observed patterns of diversity by means of generalized linear mixed models.ResultsAn overall pattern of higher genetic diversity was found in the deeper sites of the Atlantic Ocean and the Mediterranean Sea. This pattern was largely explained by bottom temperatures, with a linear pattern of decreasing genetic diversity with increasing thermal stress. Genetic differentiation patterns showed higher gene flow within sites (i.e., shallow vs. deeper populations) than between sites. Recent genetic bottlenecks were found in two populations of shallow depths.DiscussionOur results highlight the role of deep refugial populations safeguarding higher and unique genetic diversity for marine structuring species. Theoretical regression modelling demonstrated how thermal stress alone may reduce population sizes and diversity levels of shallow water populations. In fact, the examination of time series on a daily basis showed the upper water masses repeatedly reaching lethal temperatures for P. clavata. Differentiation patterns showed that the deep richer populations are isolated. Gene flow was also inferred across different depths; however, not in sufficient levels to offset the detrimental effects of surface environmental conditions on genetic diversity. The identification of deep isolated areas with high conservation value for the red gorgonian represents an important step in the face of ongoing and future climate changes.

Dataset Information

Population collapse of habitat-forming species in the Mediterranean: a long-term study of gorgonian populations affected by recurrent marine heatwaves.

Publications

Population collapse of habitat-forming species in the Mediterranean: a long-term study of gorgonian populations affected by recurrent marine heatwaves.

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