Conservation of marine habitat-forming species under climate change: population genetics and demographic responses of the Mediterranean red gorgonian Paramuricea clavata.

Abstract

Climate change, along with other anthropogenic pressures (e.g. water pollution, overfishing and habitat degradation), is severely impacting oceans around the world, producing important changes in its physical and biological structure, and causing marine biodiversity to decline. In this context, the enhancement of conservation and management strategies that mitigate such stressors (e.g. Marine Protected Areas, MPAs) is urgent. In this thesis, we studied the population genetics and ecological responses to warming of the Mediterranean red gorgonian Paramuricea clavata (Risso 1826), in order to contribute to the design of more effective conservation and management measures for this and other similar species. P. clavata is a long-lived, slow-growing, low dispersal and highly vulnerable habitat-forming organism from the coralligenous assemblages. During the last decades, it has been severely impacted by mass mortality events (MME) caused by climate change-related thermal anomalies. P. clavata is essential to maintain biodiversity as it forms habitat for other organisms and it greatly contributes to habitat's biomass and complexity. Although the inclusion of habitat formers in the design of MPAs is fundamental to improve the effectiveness of biodiversity protection, these organisms have been generally neglected in the planning of MPAs, which, instead, have been historically designed for the protection of commercially important species.

In this thesis, we developed an interdisciplinary approach focused on (i) population genetics, emphasizing on evolutionary processes acting over contemporary timescales, and (ii) on demographic responses to warming. First, we compared the functioning of continuous and isolated metapopulations of P. clavata, in terms of spatial genetic structure and underlying evolutionary processes. A group of genetically differentiated populations was detected in a geographically continuous area, indicating that in addition to geographic isolation, genetic isolation should also be considered in the design of MPAs. Genetically isolated metapopulations exhibited significantly lower genetic diversity and higher genetic differentiation compared to continuous metapopulations. Moreover, the influence of drift was higher in isolated metapopulations. These results suggest that isolated metapopulations may be at higher extinction risk than their continuous counterparts. Second, we used an eco-evolutionary approach combining demographic and genetic data to establish conservation priorities in an isolated metapopulation. We demonstrated a relation between partial mortality (caused by MME), effective population size (Ne) and number of alleles that indicated that the less diverse and most isolated demes, which were undergoing the largest effect of drift, were the most affected by MME. These populations should therefore be of high conservation priority. We detected a newly established population, which was also prioritized for conservation, as it was mainly composed by juvenile colonies. Surprisingly, no founder effect was observed, as its genetic diversity was high and colonies came from different populations Third, we experimentally tested the role of reproductive maturity and sex on the vulnerability of the red gorgonian to warming. The highest vulnerability of adults versus juveniles and of females versus males results in a decline of fertilization rates, larval production and recruitment success, suggesting that red gorgonian populations may collapse in a warmer future.

The relevance of our results is discussed in the light of climate change, and several conservation and management strategies that should be implemented to enhance the conservation of P. clavata and its associated communities are proposed. Moreover, this thesis provides valuable information to improve the effectiveness of MPAs within the context of climate change and it strengthen the previous foundations of knowledge that are essential to pursue further research. Given the key role of P. clavata as a habitat former, the results obtained in this work may also serve as guidelines to enhance the protection of other habitat-forming species with similar life history traits.

El cambio climático y otras amenazas antrópicas están afectando gravemente la biodiversidad marina. El diseño de medidas de conservación que mitiguen la acción de dichos impactos (e.g. Áreas Marinas Protegidas, AMPs) es, entonces, urgente. Usando un enfoque interdisciplinar, en esta tesis nos enfocamos en la gorgonia mediterránea Paramuricea clavata, con el fin de mejorar las estrategias de gestión y conservación de ésta y otras especies similares. P. clavata es una especie formadora de hábitat del coralígeno, que por presentar una lenta dinámica poblacional y tener una baja capacidad de dispersión, es muy vulnerable a las perturbaciones. Por ejemplo, en las últimas décadas, ha sufrido severas mortalidades masivas causadas por anomalías térmicas relacionadas con el cambio climático. En esta tesis, inicialmente comparamos el funcionamiento de metapoblaciones aisladas o continuas en términos de genética de poblaciones. Se encontró un grupo de poblaciones genéticamente aisladas dentro de una metapoblación geográficamente continua, indicando que el aislamiento genético debe ser clave en el diseño de AMPs. Las metapoblaciones aisladas presentaron una variabilidad y una diferenciación genética significativamente menor y mayor, respectivamente, que las metapoblaciones continuas, así como una influencia significativa de la deriva genética, indicando que las metapoblaciones aisladas pueden ser menos resilientes que las continuas. Luego, utilizamos un enfoque eco-evolutivo para priorizar poblaciones para la conservación en una metapoblación aislada. Las poblaciones menos diversas y más aisladas fueron priorizadas, debido a su mayor mortalidad parcial y al fuerte efecto de la deriva genética. Una población recientemente fundada, compuesta principalmente por juveniles y donde no se detectó un efecto fundador, también se identificó como prioritaria. Por último, evaluamos experimentalmente el efecto de la madurez reproductiva y el sexo en la vulnerabilidad de P. clavata al calentamiento del mar. La mayor vulnerabilidad de los adultos versus los juveniles y de las hembras versus los machos tiene graves consecuencias para la persistencia de esta especie en un futuro con mayor calentamiento, ya que el esfuerzo reproductivo es drásticamente afectado por las altas temperaturas. Esta tesis aporta información valiosa para mejorar la conservación de P. clavata y sus comunidades asociadas, así como para incrementar la efectividad de AMPs.