Unveiling Asexual Reproductive Traits in Black Corals
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Unveiling asexual reproductive traits in black corals: polyp bail-out in Antipathella subpinnata Martina Coppari, Lara Fumarola, Lorenzo Bramanti, Pascal Romans, Rémi Pillot, Giorgio Bavestrello, Marzia Bo To cite this version: Martina Coppari, Lara Fumarola, Lorenzo Bramanti, Pascal Romans, Rémi Pillot, et al.. Unveiling asexual reproductive traits in black corals: polyp bail-out in Antipathella subpinnata. Coral Reefs, Springer Verlag, 2020, 39, 10.1007/s00338-020-02018-1. hal-02986281 HAL Id: hal-02986281 https://hal.archives-ouvertes.fr/hal-02986281 Submitted on 25 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Coral Reefs https://doi.org/10.1007/s00338-020-02018-1 NOTE Unveiling asexual reproductive traits in black corals: polyp bail- out in Antipathella subpinnata 1,2 3,4 4 5 Martina Coppari • Lara Fumarola • Lorenzo Bramanti • Pascal Romans • 5 1,2 1,2 Re´mi Pillot • Giorgio Bavestrello • Marzia Bo Received: 22 June 2020 / Accepted: 14 October 2020 Ó The Author(s) 2020 Abstract Cnidarians are known to undergo reverse Introduction development as a survival mechanism against adverse environmental conditions. Polyp bail-out consists in the Polyp bail-out, the active detachment of polyps from the polyps’ detachment from the mother colony due to stressful mother colony (Sammarco 1982), is an extreme response conditions, followed by a complete tissue and cells rear- serving as a survival and escape strategy under unfavorable rangement and in some cases in a regression into a simple, environmental conditions, which could lead to the death of ciliated form. Here we describe a massive polyp bail-out the mother colony (Peter III et al. 2014; Fordyce et al. event occurred in the mesophotic black coral Antipathella 2017). Polyp bail-out represents an example of reverse subpinnata in reared conditions. This is the first report of a development (Piraino et al. 2004) in which a detached bail-out event in this species providing new insights into polyp undergoes complete tissue and cell rearrangement the life cycle and ecology of black corals. with loss of the compartment structure present in the pri- mary polyp (Kariyazono and Hatta 2015). Until now, this Keywords Antipatharians Á Asexual reproduction Á Bail- phenomenon has been described only in aquaria, even out Á Aquaria though its presence is hypothesized in natural conditions (Miller and Grange 1997). Indeed, the capability of cnidarians to undergo polyp bail-out highlights their high plasticity to shift from a Topic Editor Anastazia Teresa Banaszak colonial to a solitary form and vice versa (Kvitt et al. 2015) and, for many Anthozoa, from a sessile to a motile form, Electronic supplementary material The online version of this escaping unsuitable environments or interspecific compe- article (https://doi.org/10.1007/s00338-020-02018-1) contains sup- plementary material, which is available to authorized users. tition (Lee et al. 2012), thus enabling survival in extreme conditions. & Martina Coppari The process of bail-out differs from polyp expulsion, [email protected] which is an asexual reproductive strategy occurring in 1 physiologically healthy coral and regulated by the parent Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Universita` degli studi di Genova, Genoa, Italy colony (Kramarsky-Winter et al. 1997). The species able to produce bail-out propagules studied 2 CoNISMa, Rome, Italy 3 so far include shallow tropical (Sammarco 1982, Capel Dipartimento di Scienze e Tecnologie Biologiche e et al. 2014; Shapiro et al. 2016; Fordyce et al. 2017) and Ambientali, Universita` del Salento, Lecce, Italy ˇ 4 temperate scleractinians (Kruzic 2007; Serrano et al. 2018), CNRS-Sorbonne Universite´, Laboratoire d’Ecoge´ochimie des as well as deep cold-water and tropical octocorals (Rakka Environnements Benthiques, LECOB, Observatoire Oce´anologique de Banyuls sur Mer, Banyuls-sur-Mer, France et al. 2019; Wells and Tonra 2020). This phenomenon occurs or can be mechanically induced (e.g., by cutting the 5 Service Mutualise´ d’Aquariologie, Observatoire Oce´anologique de Banyuls, FR3724. Sorbonne Universite´ tentacles) also in antipatharian species (Parker et al. 1997; CNRS, Banyuls-sur-Mer, France Bo 2008; Gonc¸alves 2016). 123 Coral Reefs Antipathella subpinnata (Ellis and Solander, 1786) is the measured, preserved in small beakers filled with filtered most frequent black coral species of Mediterranean Tem- seawater (0.2 lm) and monitored every 3 days for 45 days. perate Mesophotic Ecosystems (TMEs) (i.e., communities Scanning Electron Microscope (SEM) observations found below PAR 1%, approximately between 40 and were performed to examine the propagules external struc- 260 m depth) (Bo et al. 2019a; Cerrano et al. 2019). It ture including their cnidome. forms forest-like aggregations (animal forest, sensu Rossi Histological examination after resin inclusion was also et al. 2017), providing a tridimensional habitat and refuge performed to study the internal structure of the propagules: or nursery area for many associated species (Bo et al. samples were fixed in 70% ethanol and then dehydrated in 2019b). A. subpinnata is gonochoric, reproduces sexually a graded ethanol series followed by inclusion in a cold- at the end of summer (Gaino and Scoccia, 2010) and curing resin and finally mounted on plastic supports. The asexually through fragmentation (Coppari et al. 2019). sections (9 lm thick) obtained by a microtome were col- Until now, asexual reproduction has been observed only in ored with Toluidine blue, then analyzed on a compound aquaria, but its presence in natural environments could not microscope. be excluded (Costantini et al. 2019). Considering that no detailed description of the bail-out process exists for antipatharians, in the present paper, we Result and discussion describe for the first time, this phenomenon in A. subpin- nata, under controlled conditions. One month after the transport to the aquarium facilities, colonies started to form motile and negative buoyant bail- out propagules (ESM 1). The process started with coeno- Materials and methods sarc withdrawal from the apical branches of the mother colony, followed by detachment from the skeleton and Six Antipathella subpinnata colonies (height ranging subsequent expulsion and ended with the formation of free- between 50 and 80 cm) were sampled in Bordighera (43° living propagules (Fig. 2a; ESM 1). The portion of the 46.110 N; 7° 40.820 E) at 63 m depth on July 9, 2018 colony releasing propagules underwent necrosis and con- (Fig. 1a). Immediately after sampling, each of the colonies secutive death. In addition to necrosis and polyp bail-out, was placed at the bottom of a tank (144 L) filled with we observed fragmentation of mother colonies’ branchlets. seawater collected at 60 m depth by a 10L Niskin bottle Moreover, gamete reabsorption, by two of the six colonies and kept at constant temperature (T =14°C, same as the that were fertile at the time of sampling, was observed by sampling site) during the transport. After approximately means of polyps’ dissection and histology. The bail-out 10 h, colonies were transferred to Banyuls-sur-Mer phenomenon was massive, with hundreds of propagules Aquarium facilities (Biodiversarium) and positioned in an produced daily; thus, dissecting microscope observations open circuit 2000-L tank (Fig. 1b) filled with filtered were performed on a subsample of 2585 randomly selected (0.2 mm) seawater taken at 20 m depth. Constant tank propagules. Four main morphologies were observed temperature (14 °C) was ensured by both a refrigerator (Fig. 2b): circular (74%, n = 1915); elongated (13%, system and a thermostatic room also equipped with blue n = 335); polypoid (10%, n = 248) (Fig. 2b); and ‘‘other’’ lights to simulate the natural light regime (0–5 lmol m-2 (3%, n = 87). Regardless of the morphology, all propa- s-1; photoperiod: 12 h day and 12 h night). Two sub- gules were actively moving by rotation on multiple axes mersible water pumps were used to ensure water move- (ESM 1). Hundred propagules for each shape were mea- ment; salinity and temperature were checked daily, while sured, and results are listed in Table 1. the ratio of NH3/NH4 and the values of NO2,NO3,PO4,pH Most of the propagules assumed the circular morpho- and copper were checked once per month. Colonies were logy (Fig. 2c). Nearly all selected propagules survived for fed twice a day with Artemia nauplia and Rotifera. the whole period of observation; however, settlement has To catch the propagules, the main aquarium wastewater never been observed. passed through a PVC cylinder equipped with a 0.2 mm net The histological analysis allowed a description of the (propagules trap) placed in a tank on the side of the main internal anatomy of all propagules types (Fig. 3a–c). The tank. Bail-out propagules retrieved in the trap were col- shape of the circular propagule in transversal section sug- lected and observed with a dissecting microscope to study gests it was either a fragment of a tentacle or a later their morphology. Propagule size was measured from pic- developmental stage of the elongated or polypoid shape. tures using the software Fiji-ImageJ (Schindelin et al. The elongated propagule, in longitudinal section, had a 2012). To quantify variability in shape and survival, 10 cylindrical shape, with a rounded distal end and an bail-out propagules were randomly collected every day, enlarged base, suggesting it derived from a whole tentacle (base included) detached from a polyp. The polypoid shape 123 Coral Reefs Fig.