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Reproductive Behavior of the Marine Gastropod Charonia Seguenzae (Aradas & Benoit, 1870) in Captivity

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Reproductive Behavior of the Marine Gastropod Charonia Seguenzae (Aradas & Benoit, 1870) in Captivity Research Article Mediterranean Marine Science Indexed in WoS (Web of Science, ISI Thomson) and SCOPUS The journal is available on line at http://www.medit-mar-sc.net DOI: http://dx.doi.org/10.12681/mms.14917 Reproductive behavior of the marine gastropod Charonia seguenzae (Aradas & Benoit, 1870) in captivity Chrysa K. DOXA1, 2, Aspasia STERIOTI1,3, Pascal DIVANACH1,3 and Maroudio KENTOURI2 1 Cretaquarium, Hellenic Centre for Marine Research, P.O. Box 2214, 71003 Heraklion, Crete, Greece 2 Biology Department, University of Crete, P.O. Box 1470, 71110 Heraklion, Crete, Greece 3 Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, P.O. Box 2214, 71003 Heraklion, Crete, Greece Corresponding author: [email protected] Handling Editor: Mehmet YOKES Received: 15 November 2017; Accepted: 17 December 2018; Published on line: 22 April 2019 Abstract The reproductive behavior of the marine gastropod Charonia seguenzae (Aradas & Benoit, 1870) was studied through the description of 19 copulation and 21 egg-laying events of 134 wild individuals. Findings in the present study regarding the re- production temperature range (20 to 23oC) and demonstration of maternal care provided important information on the biology, behavior, and ecology of this species. Furthermore, observed polyandry by females and the collaborative care of embryonic sacks were two aspects of the reproductive biology of this species that pose new questions both at the ecological and evolutionary level. Keywords: Charonia seguenzae; reproduction; behavior; maternal care; polyandry. Introduction released back into the sea (Katsanevakis et al., 2008). The re-establishment of Charonia stocks in depleted The triton Charonia seguenzae (Aradas & Beno- areas requires strong knowledge of the biology and ecolo- it, 1870), formerly reported as C. variegata (Clench & gy of this genus, which can be supplemented by the study Turner, 1957) or C. tritonis variegata (Beu, 1970), was of captive populations. As such, interest in the rearing of only recently classified as a separate species of the East- Charonia species for bio-manipulation and ecological ap- ern Mediterranean Sea (Beu, 2010). Scientific knowl- plications has increased in recent years (Doxa et al., 2012, edge related to its biology is scarce and focuses mainly 2013; Zhang et al., 2013; Cavallaro et al., 2016; Kang et on geographical distribution, taxonomy (Beu, 2010), and al., 2016; Bose et al., 2017). Firm knowledge regarding captive feeding (Doxa et al., 2012; 2013). Complemen- reproductive behavior is a prerequisite for the breeding tary literature from the Indo-Pacific zone provides some of a species. Prosobranch gastropods are generally gono- biochemical and pharmacological data (Teshima et al., choristic, and fertilisation is internal in most cases. Most 1979) as well as findings on the feeding and reproductive of the Caenogastropoda, including all Ranellidae species, behavior (Laxton, 1969, 1971; Birkeland & Lucas, 1990; enclose their eggs in capsules, which provides protection Kang & Kim, 2004) of Charonia sp. individuals in tropi- from radiation as well as mechanical and osmotic stress cal and subtropical waters. and predators (Pechenik 1978, 1979, 1982, 1983, 1986; Previously abundant, populations of Charonia species Perron, 1981; Lord, 1986; Hawkins & Hutchinson, 1988; are declining or extinct in some cases due to over-fish- Pauly & Pullin, 1988; Rawlings, 1996). ing for food and ornamental purposes (Russo et al., 1990; Parental care consists of a wide range of behavioural, Hosking, 1996; Wang, 1997; McLean, 1999; Kang & Kim, morphological, and physiological responses that have 2004; Katsanevakis et al., 2008). Currently, although not evolved in most taxa to increase offspring survival. Most listed under the IUCN Red List (2009), both Charonia studies have focused on parental care in vertebrates, while species existing in the Mediterranean Sea (C. lampas and the ecology and evolution of parental care of many inver- C. seguenzae) are protected according to Annex II of the tebrate taxa remain un- or understudied (Clutton-Brock, Bern Convention (Council of Europe, 1979) and the Pro- 1991). Gastropods present a large variety of parental care tocol of the Barcelona Convention (European Communi- adaptations. Some of these adaptations include the en- ty, 1999). However, individuals caught in nets are rarely closure of unfertilised eggs (nurse eggs) within egg cap- Medit. Mar. Sci., 20/1, 2019, 49-55 49 sules, the incubation of the egg capsules under the foot, the experiment. the preparation of surfaces for capsule deposition, the attachment of egg capsules on the parental shell, the stor- age of eggs in the mantle cavity, and even ovoviviparity Experimental procedure and viviparity (Purchon, 1977; Tompa et al., 1984; Baur, 1994; Kamel & Grosberg, 2012). The reproductive behavior of the marine gastropod C. The reproductive behavior of C. seguenzae has not seguenzae was described for the populations held in the been previously described, while some aspects of re- quarantine area of Cretaquarium from 2007-2011. The productive behavior of other Charonia species from the observations included the daily monitoring (from 8:00 Western Mediterranean Sea and Indo-Pacific Ocean have to 16:00) of all animals and the recording of copulation been documented (Laxton, 1969; Zhang, 2013; Cavallaro events (time, duration), egg capsule depositions, and the et al., 2016). The aim of the present study is to enrich behavior of the animals in the tank. It was not possible the existing knowledge and offer a thorough and detailed to record nocturnal animal behavior due to facility lim- description of the reproductive behavior of C. seguenzae. itations. The experimental aquaria were in the aquarium quarantine area with other fish under the same photope- riod. During scotophase, the lighting conditions were not Materials and Methods suitable for recording. The individuals were identified either by an engraved number (Dremel 400 Digital) on their shell (Fig. 1) or by distinct morphological differenc- Experimental population and holding conditions es and shell markings. Experiments were conducted over a four-year period (2007-2011) at the facilities of Cretaquarium, a public aquarium of the Hellenic Centre for Marine Research (HCMR). Divers hand-picked 134 specimens of Char- onia seguenzae from the inshore littoral zone of Crete, Greece, which were transported to the facility. Specimens were divided into groups of 5-10 individuals and were placed in 150 and 300L aquaria. During this period, food was provided once a week and consisted of frozen sea stars, fish, as well as live sea urchins and holothurians. Aquaria were organised as semi-closed circuits with air- lift as well as mechanical and biological filtration. Aquar- ia were filled with seawater (35‰) from a deep circum- littoral borehole. Water renewal and recirculation rates were 30 and 100 %/h, respectively. White 60 W neon lamps were used for illumination, with photoperiod ad- justed to 13L-11D. Temperature was regulated through a o heat exchange system at 20 and 23 C, and 67 individuals Fig. 1: Engraved number (encircled area) used as identification were held under each regime. Oxygen saturation (above mark on a Charonia seguenzae shell. 90%) and pH (7.7 ± 0.1) remained constant throughout Fig. 2: A) Copulation of Charonia seguenzae: Female - bottom left, male - upper right. B) Copulation of a male Charonia seguen- zae with a female that had already deposited egg capsules. 50 Medit. Mar. Sci., 20/1, 2019, 49-55 Results 4 days, while the interval between batches ranged from 1 to 24 days. The capsules were placed next to each oth- er, lacking any obvious pattern, and the different batches Copulation were placed either next to each other, among each other, or at completely different sites in the tank. Fertilisation was internal, with the male usually at- tached to the female’s shell, inserting its penis into the female’s mantle cavity (Fig. 2A). A total of 19 copulation Maternal care events were recorded. The copulation, lasting 2-4 hours per session, took place early in the morning. It was not Strong maternal behavior was observed during incu- possible to estimate the exact copulation duration, since bation period, since the female remained in the depositing copulation likely began during the night and was only re- area to protect the capsules and clean them from parasites corded early in the morning. It is also possible that not and algae. The cleaning process included the extension of every copulation event was recorded if it occurred entire- the mother’s proboscis and the ‘licking’ of the capsules ly during the night. (Fig. 5B). Mothers were dedicated to their egg capsules Egg capsule deposition was observed from day 3 sites, with occasional short break intervals lasting from to day 95 after fertilisation with a male being observed 1 hour to 3 days. Most of these breaks occurred during copulating with a female that had already deposited egg feeding. The mothers ate once per month during this peri- capsules (Fig. 2B). On three occasions, a female copulat- od, even though food was provided once per week. ed with different males at separate times. On one occa- Apart from the mothers, other individuals in the same sion, the simultaneous copulation of one female with two tank provided care to the egg capsules in 16 out of 21 males was recorded, with both males being attached to (76%) observed depositions. During the developmental the female’s shell and both having inserted their respec- period, one to five other individuals were present in the tive penises into the female’s mantle cavity (Fig. 3) for deposition area (Fig. 6). Their presence was not continu- over 2 hours (135 min). ous and lasted 1 to 3 days On two occasions, a male that was copulating with a female after her first deposition was observed cleaning the capsules using its proboscis Egg capsule deposition in the same manner as the females (Fig. 5). Furthermore, on another two occasions, two females that had deposited Between 2007 and 2011, 21 egg capsule depositions capsules in the same aquarium during the same period took were observed and studied.
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