Internship Report

INTERNSHIP REPORT Impact of the nudibranch Doris verrucosa predation on the sponge Hymeniacidon perlevis community dynamics By Clémence Potel Supervised by María López-Acosta Sept.-Dec. 2020 • Acknowledgement I would like to thank María López-Acosta who was a wonderful internship tutor. She let me work alongside her in this project, made me discover the world of a marine biologist researcher and gave me great advice for the writing of this report. I would also like to thank Aude Leynaert (and Marguerite Baradat) without whom I would not have been able to do this internship neither had this lovely experience; the divers Isabelle Bihannic, Erwan Amice and Thierry Le Bec for their sympathy and letting me sail with them; and the whole LEMAR institution for the warm welcome. • Abstract (English) Sponges are one of the most ancestral multicellular animals still living on earth but yet, they are still poorly studied and understood by the research community compared to other marine benthic metazoans. Sponges are known to play lots of essential roles in marine ecosystems such as stabilizing marine substrate and provide microhabitats for smaller benthic organisms as well as they are also involved in several nutrient cycles. Therefore, a better understanding of the dynamics of sponge populations could prevent potential future ecological crises. This study focuses on the impact of the nudibranch Doris verrucosa predation on the sponge Hymeniacidon perlevis in a shallow-water ecosystem in which they cohabit, the maerl beds of the Bay of Brest, France. The predation rate is estimated by the quantification of the sponge volume eaten per nudibranch volume in a day (mL sponge mL⁻¹ nudibranch D⁻¹). To do so, the sponge volume was measured by association of various geometric shapes, before and after being offered to a nudibranch for 24h. The nudibranch volume was also measured after the experience. The predation rate was then calculated by subtracting the final sponge volume to the initial one, and normalized by the nudibranch volume. The experiment has been led 5 times on 30 nudibranchs in the laboratory to investigate intra- and inter-individual variabilities and once on 10 nudibranchs in situ, to measure the predation rate in their natural habitat. From the laboratory experiments, we learnt that there was no specific intra-individual variability and that the main inter-individual activity was due to the nudibranch size. From the in situ incubations, we estimated that the average predation rate is 0.156 ± 0.091 mL sponge mL⁻¹ nudibranch D⁻¹. Then, the predation activity was extrapolated to the nudibranch population in its natural habitat from June to October (the months in which these predators are active) 2020, we found that 41.24 ± 25.12% of H. perlevis biomass is eaten by its main predator, D. verrucosa, in the maerl bed of the Bay of Brest. Therefore, D. verrucosa strongly impacts the H. perlevis population dynamics and its distribution over the year cycle. • Keywords (english): sponge, nudibranch, predator-to-prey relationship, predation rate, sponge population dynamics, marine benthic ecosystems • Abstract (Français) Les éponges font partie des animaux multicellulaires les plus ancestraux vivant encore aujourd’hui sur Terre et pourtant, elles sont peu étudiées et peu comprises par la communauté des chercheurs, contrairement à d’autres métazoaires marins benthiques. Les éponges sont connues pour jouer plusieurs rôles essentiels dans les écosystèmes marins comme la stabilisation des substrats marins mais représentent aussi des microhabitats pour les plus petits organismes benthiques et sont impliquées dans les cycles de nombreux éléments chimiques. Par conséquent, mieux comprendre les dynamiques des populations des éponges pourrait éviter de potentielles crises écologiques futures. Cette étude se focalise sur l’impact de la prédation du nudibranche Doris verrucosa sur l’éponge Hymeniacidon perlevis dans leur écosystème naturel, les lits de maërl en eaux peu profondes de la Rade de Brest, France. Le taux de prédation est estimé par la quantification du volume d’éponge mangé par volume de nudibranche et par jour (mL éponge mL⁻¹ nudibranche J⁻¹). Pour y parvenir, le volume d’éponge fut mesuré deux fois par association de différentes formes géométriques: avant et après qu’elle fût offerte au nudibranche pendant 24h. Concernant le nudibranche, son volume fût mesuré à la fin de l'expérience suivant la même technique. Le taux de prédation fût calculé en soustrayant le volume final de l'éponge à son volume initial, et divisé par le volume du nudibranche. Cette expérience a été menée en laboratoire 5 fois sur 30 nudibranches, et une fois in situ sur 10 nudibranches afin de calculer le taux de prédation dans l’habitat naturel des organismes d’étude. À partir des expériences menées en laboratoire, nous avons découvert qu’il n’y a pas de variabilité intra-individuelle particulière mais que la principale variabilité inter-individuelle est due à la taille du nudibranche. À partir des expériences in situ, nous avons estimé un taux de prédation moyen de 0.156 ± 0.091 mL éponge mL⁻¹ nudibranche J⁻¹. Ensuite nous avons extrapolé notre résultat sur la population des nudibranches dans habitat naturel entre Juin et Octobre (ce qui représente la saison d’activité des nudibranches) 2020 et avons trouvé que 41.24 ± 25.12% de la biomasse de H. perlevis a été mangé par son principal prédateur D. verrucosa dans le lit de maërl de la Rade de Brest. Par conséquent, D. verrucosa impacte fortement les dynamiques et la distribution de la population de H. perlevis. • Keywords (français): éponge, nudibranche, relation proie-prédateur, taux de prédation, dynamiques de population des éponges, écosystèmes marins benthiques • Graphical abstract • Introduction Marine sponges are conspicuous animals in benthic ecosystems. Their large spectrum of species make them ubiquitous in marine environments, regardless of latitude and depth, forming in some cases enormous aggregations that may extend over large areas [1]. Sponges play several functional roles in the global marine ecosystem such as substrate stabilization or microhabitats for other benthic organisms. They are also involved in several nutrient cycles essentially silicon, carbon and nitrogen [2,3]. Thus, understanding the dynamics of sponge populations is important to acknowledge the global marine ecosystem functioning and to prevent potential risks to which marine ecosystems could be exposed. Sponges are known to be poorly predated [4,5]. This feature is due to their mineral skeleton. Most sponge species build their skeletons with mineral material, either carbonate calcium or amorphous silica. Some sponge species combine their mineral skeletons with organic compounds, which are mainly made by spongin, a collagenous-like protein [6]. The whole skeleton causes irritation of their predators’ mouth and gut and the spongin protein is known to be very indigestible for most marine animals. Additionally, certain species of sponges produce chemical toxins in order to deter predators from feeding [7]. The few main sponge predators which have been reported are sea stars, angelfishes, trunkfishes, file fishes and nudibranchs [4,5,7]. To date, most of the studies on sponge predation have been conducted in tropical latitudes, particularly in the Caribbean coral and sponge reefs [4,5,7,8], with only some studies in high latitude environments [9]. Surprisingly, there are hardly any studies on sponge predation in temperate latitudes [10]. This represents a lack of information concerning the sponge communities, given that not only their diversity and role but also the benthic population dynamics highly change across latitudes [11,12]. Here we have studied nudibranchs’ predation on sponges in the Bay of Brest, France (NW Atlantic). Nudibranchs, also called “sea slugs”, are shell-less invertebrate molluscs. Depending on the species or the family, they feed on a specific kind of prey [13]. For instance, some species, such as those belonging to the Family Dorididae, are spongivores [14]. Along evolution, they have become unaffected to sponges’ secondary metabolites. Two main types of spongivorous exist: the specialists, which only feed on one specific sponge species, therefore they are adapted to predation on this species and are totally unaffected by its defense system. For instance, a correlation between certain nudibranchs’ tooth concavity and certain sponges’ spicules shows a specific adaptation for predation [15]. The second type of spongivores are generalists which feed on several sponges species. Either because they are looking for different sorts of nutrients, either to limit recurrent damages caused by one specific defense mechanism, or simply because they are not affected by any of the sponges’ secondary metabolites [4]. The nudibranch of interest in our study, Doris verrucosa belongs to the family Dorididae and follows the last case scenario: it has mainly been observed feeding on Hymeniacidon perlevis (formerly called Hymeniacidon sanguinea) but sometimes on other sponge species [16]. In this study we focus on the predator-to-prey relationship between the nudibranch D. verrucosa and the sponge H. perlevis by determining the predation rate (i.e., quantity and velocity of sponge biomass eaten by nudibranchs) and consequently, the impact that the nudibranchs have, through predation, on the sponge population

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