Synchronized Broadcast Spawning by Six Invertebrates (Echinodermata and Mollusca) in the North-Western Red Sea
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Research Collection Journal Article Synchronized broadcast spawning by six invertebrates (Echinodermata and Mollusca) in the north-western Red Sea Author(s): Webb, Alice E.; Engelen, Aschwin H.; Bouwmeester, Jessica; van Dijk, Inge; Geerken, Esmee; Lattaud, Julie; Engelen, Dario; de Bakker, Bernadette S.; de Bakker, Didier M. Publication Date: 2021 Permanent Link: https://doi.org/10.3929/ethz-b-000479154 Originally published in: Marine Biology 168(5), http://doi.org/10.1007/s00227-021-03871-6 Rights / License: Creative Commons Attribution 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Marine Biology (2021) 168:56 https://doi.org/10.1007/s00227-021-03871-6 SHORT NOTES Synchronized broadcast spawning by six invertebrates (Echinodermata and Mollusca) in the north‑western Red Sea Alice E. Webb1 · Aschwin H. Engelen2 · Jessica Bouwmeester3,4 · Inge van Dijk5 · Esmee Geerken1 · Julie Lattaud6 · Dario Engelen1,2,3,4,5,6,7,8 · Bernadette S. de Bakker7 · Didier M. de Bakker8 Received: 26 November 2020 / Accepted: 21 March 2021 © The Author(s) 2021 Abstract On the evenings of June 11 and 12, 2019, 5 and 6 days before full moon, broadcast spawning by four echinoderm species and two mollusc species was observed on the Marsa Shagra reef, Egypt (25° 14′ 44.2" N, 34° 47′ 49.0" E). Water temperature was 28 °C and the invertebrates were observed at 2–8 m depth. The sightings included a single basket star Astroboa nuda (Lyman 1874), 2 large Tectus dentatus (Forskal 1775) sea snails, 14 individuals of the Leiaster cf. leachi (Gray 1840) sea star and 1 Mithrodia clavigera (Lamarck 1816) sea star, 3 Pearsonothuria graefei (Semper 1868) sea cucumbers, and 2 giant clams, Tridacna maxima (Röding 1798). The observations presented here provide relevant information on broadcast spawning of non-coral invertebrate taxa in the Red Sea, where spawning is considerably less well documented than in other tropical geographical regions such as the Indo-Pacifc and Caribbean. Introduction amongst reef populations (Atchison et al. 2008; Nunes et al. 2011). Broadcast spawning occurs across most marine phyla The sedentary nature of many invertebrates on coral reefs (e.g. Hagman and Vize 2003; Ritson-Williams et al. 2005; renders them heavily reliant on dispersal during the pelagic Hofman et al. 2011; Bouwmeester 2013) and is a mode of larval period of their life cycle to ensure connectivity reproduction in which large quantities of male and female gametes are released into the water column within a short period of time. Success of the strategy, however, relies on Responsible Editor: J. Grassle Reviewers:undisclosed experts. reproductive synchrony among intraspecifc individuals within a few hours of specifc nights each year. Such annual * Didier M. de Bakker [email protected] spawning events have been shown to be closely tied to fac- tors such as annual temperature variation, lunar cycles and 1 Department of Ocean Systems, NIOZ-Royal Netherlands photoperiod length (Boch et al. 2011; Sweeney et al. 2011; Institute for Sea Research, and Utrecht University, Keith et al. 2016). To date, Invertebrate species other than 1790 AB Den Burg, The Netherlands scleractinian corals have received noticeably less attention 2 Centro de Ciências Do Mar Do Algarve (CCMAR), with regard to reproduction and this is particularly relevant University of Algarve, 8005 139 Faro, Portugal for the Red Sea, where only very few studies have been con- 3 Smithsonian Conservation Biology Institute, National ducted on multi-species broadcast spawning (Bouwmeester Zoological Park Department, Front Royal, VA 22630, USA et al. 2016). Here we describe spawning observations of 23 4 Hawaii Institute of Marine Biology, Kaneohe, HI 96744, non-coral invertebrates belonging to six species and two USA phyla. 5 Alfred-Wegener-Institut, Helmholtz-Zentrum Für Polar-Und Meeresforschung, 27570 Bremerhaven, Germany 6 Biogeoscience Group, ETH Zurich, 8092 Zurich, Switzerland Materials and methods 7 Department of (Neuro)Pathology, Amsterdam UMC, University of Amsterdam, 1105AZ Amsterdam, On the evenings of June 11 and 12, 2019 at 19:00–20:30 h, The Netherlands broadcast spawning by six invertebrate species (Mollusca 8 Wageningen Marine Research, Wageningen University and Echinodermata) was observed on the Marsa Shagra reef, and Research, 1780 AB Den Helder, The Netherlands Vol.:(0123456789)1 3 56 Page 2 of 6 Marine Biology (2021) 168:56 Egypt (~ 25 km north of Marsa Alam, 25° 14′ 44.2" N 34° 47′ were encountered releasing a jet of male gametes into the 49.0" E). This fringing reef is characterized by a wide (~ 1 water column (Fig. 1b). They were found 10 m apart, both 000 m) and shallow (< 1 m at high tide) reef fat underlain by perched on top of a coral mound (Table 1). a large carbonate framework. The reef fat is interrupted by a On June 12, 14 starfsh Leiaster cf. leachi (Gray 1840) sand channel (bay) shouldered by gradually downward slop- were seen broadcast spawning. Several individuals released ing reefs on both sides, and which transitions into a reef shelf sperm, while other individuals were observed releasing a at ~ 20 m depth. All spawning was observed on the sloping cloud of eggs (Table 1). Individuals were several meters apart edges of the channel at 2–8 m depth (Table 1). The reef slope from each other (i.e. no clustering) and generally on top of is characterized by a complex structural morphology and a coral mounds. Most of them exhibited the same spawning 60–70% cover of scleractinian coral (mainly Acropora spp., behaviours with raised discs and perched on the tips of their Porites spp. and Pocillopora spp., pers. obs. DdB). Water tem- arms (Fig. 1c). Another sea star species, Mithrodia clavigera perature at 5 m depth was 28 °C, measured with a Suunto D4i (Lamarck 1816), was encountered releasing male gametes in dive computer. All observations were made while SCUBA a fattened position on top of a coral mound (Table 1). diving and an underwater photographic record was taken for During the same evening, spawn was observed emanat- each observation. Species identifcation, and the identifcation ing from three Pearsonothuria graefei (Semper 1868) sea of sperm or egg spawn, was performed visually in situ. Sperm cucumbers (Table 1). One was observed on a sandy bot- release was characterized by a “smoky” cloud emitted by the tom with half of its body lifted of the seafoor in a vertical individuals, and egg release was characterized by a “non- position. It swayed with the waves’ surging motion while smoky” cloud of tiny conspicuous eggs. Taxonomic identi- releasing a cloud of male gametes. The two other individu- fcations were later confrmed by Gustav Paulay (FLMNH, als were encountered briefy emerging from the cryptic reef USA) based on the extensive photographic and video mate- environment to release a single cloud of male gametes before rial. Due to permit limitations and the limited number of indi- rapidly retreating into the reef (ESM_1). Lastly, two giant viduals that were observed spawning, no voucher specimens clams (Tridacna maxima, Röding 1798) were encountered, were collected for posteriori identifcation. releasing a cloud of male gametes. Discharge lasted for only a few seconds and occurred through the excurrent siphons. The two individuals were in close proximity (1 m apart), Results embedded in the same coral mound. They spawned within seconds of each other (ESM_1). Spawning observations A single basket star, Astroboa nuda (Lyman 1874), was Discussion observed on June 11 perched on top of a fre coral releas- ing female gametes (Fig. 1a, Table 1). When encountered, Spawning times of four out of the six species encountered the individual was in a typical feeding position with arm here were not yet described for the Red Sea and to our branches extended and was releasing a vast number of eggs knowledge, this is the frst feld observation of a basket star (~ 1 mm diameter) that were dispersed by the prevailing cur- releasing female gametes. Relatively little is known about rent. When illuminated, it continued spawning but drew in the life history of A. nuda, but our observations suggest that its arms towards the central disk, which is typical for this this species—like many Ophiuroids—relies on broadcast extremely light-sensitive species (Tsurnamal and Marder spawning. Apart from our description of mass egg release 1966; Hendler et al. 1995). A few minutes later, two large in the north-western Red Sea, the only other in situ descrip- top-shell snails (Trochidae), Tectus dentatus (Forskal 1775) tion of spawning appears to be a single A. nuda individual Table 1 Timetable and specifcations of the recorded invertebrate spawning Days before full moon Species Number of indi- Time of spawning Type of gametes Depth (m) viduals 6 (June 11) Astroboa nuda 1♀ 19:45 Eggs 8 Tectus dentatus 2♂ 20:00–20:10 Sperm 3–5 5 (June 12) Leiaster cf. leachi 5♂ & 9♀ 19:30–20:15 Sperm & eggs 3–8 Mithrodia clavigera 1♂ 20:15 Sperm 2 Tridacna maxima 2⚥ 19:50 Sperm 3 Pearsonothuria graefei 3♂ 19:50–20:10 Sperm 2–5 1 3 Marine Biology (2021) 168:56 Page 3 of 6 56 Fig. 1 Nocturnal spawning of non-coral invertebrates on the shallow dentatus sea snail. c Leiaster cf. leachi discharging female gametes reef of the Egyptian Red Sea. a Astroboa nuda releasing eggs. b Con- in typical upright position. Video footage of all observed species is tinuous jet-like release of male gametes from the siphon of a Tectus provided as Supplementary Resource 1 (ESM_1) releasing sperm two nights before the full moon (July 2012) 1966), and this behaviour did not appear to be afected by on the Red Sea reef Al Fahal (Saudi Arabia) (Bouwmeester their spawning activity.