Observations on the Reproductive Cycles of Some Viviparous North American Sharks

aqua, International Journal of Ichthyology Observations on the reproductive cycles of some viviparous North American sharks José I. Castro NOAA, National Marine Fisheries Service, Southeast Fisheries Science Center at Mote Marine Laboratory, 1600 Ken Thompson Pkwy, Sarasota, Florida 34236, USA. E-mail: [email protected] Received: 07 July 2009 – Accepted: 23 September 2009 Abstract gleicher Vitellogenese und Trächtigkeit sowie kontinuier- The reproductive cycle of sharks is defined by how often licher Ovulation. Squalus acanthias zeigt den dornhai-typis- a species breeds and consists of two periods: vitellogenesis chen zweijährigen Fortpflanzungszyklus mit parallel and gestation. These two periods can run concurrently or laufender Vitellogenese und Trächtigkeit. Die Haie der Gat- consecutively, and the duration of each period is variable. tungen Carcharhinus, Sphyrna (teilweise) und Ginglymostoma Together, the periods of vitellogenesis and gestation deter- bekommen alle zwei Jahre Nachwuchs, Dottereinlagerung mine the length of the reproductive cycle. The genera Rhi- und Trächtigkeit folgen aufeinander. Bei Galeocerdo cuvier im zoprionodon, Mustelus, and some Sphyrna exhibit annual West-Atlantik dauert die Trächtigkeit 12 Monate, der Zyklus cycles with concurrent vitellogenesis and gestation, and insgesamt dürfte zweijährig sein. Carcharhinus obscurus hat thus, they produce one brood each year. Carcharias taurus eine 18-monatige Trächtigkeitsphase und wahrscheinlich females apparently have a biennial reproductive cycle with einen dreijährigen Fort pflan zungszyklus. Der zweijährige discontinuous ovulation. Alopias spp. exhibit an annual Zyklus mit den verschiedenen Varianten kommt also bei cycle with concurrent vitellogenesis and gestation, and have Haien unterschiedlicher stammesgeschichtlicher Herkunft continuous ovulation. Squalus acanthias has a squaloid vor, so bei Angehörigen von Carcharhinus, Squalus und Orec- biennial cycle with concurrent vitellogenesis and gestation. tolobus, er spiegelt die physiologischen Vorgänge wider, die Sharks of the genera Carcharhinus, some Sphyrna, and längere Zeit brauchen, um genügend Energie für die Pro- Ginglymostoma have a biennial cycle with consecutive vitel- duktion von Nachwuchs aufzubauen. logenesis and gestation. Galeocerdo cuvier has a 12-month gestation period in the western Atlantic, its reproductive Résumé cycle may be biennial. Carcharhinus obscurus has an 18- Le cycle de reproduction des requins est défini par le month gestation period and probably a three-year repro- nombre d’actes reproductifs d’une espèce et comprend ductive cycle. The biennial cycle, with all its variations, is deux périodes; la vitellogenèse et la gestation. Ce deux found in sharks of different phyletic origins such as car- périodes peuvent être simultanées ou consécutives et la charhinoid, squaloid, and orectoloboid sharks, reflecting durée de chaque période est variable. Ensemble, les pério - their common physiological processes that require a long des de vitellogenèse et de gestation déterminent la lon - time to accumulate sufficient energy to produce a brood. gueur du cycle de reproduction. Les genres Rhizopriono - don, Mustelus et certains Sphyrna présentent des cycles Zusammenfassung annuels avec vitellogenèse et gestation simultanées et ils Der Fortpflanzungszyklus der Haie definiert sich durch den produisent donc une progéniture par an. Les femelles de Fortpflanzungsrhythmus und besteht aus zwei Abschnitten: Carcharias taurus semblent connaître un cycle de reproduc- der Vitellogenese (Dottereinlagerung) und der Trächtigkeit. tion biennal avec ovulation discontinue. Les espèces d’Alo - Die beiden Phasen können parallel laufen oder aufeinander pias ont un cycle annuel, avec vitellogenèse et gestation folgen, und die Dauer jeder Phase ist variabel. Zusammen simultanées, et ont une ovulation continue. Squalus acan- bestimmen die beiden Abschnitte der Vitellogenese und der thias a un cycle biennal squaloïde, avec vitellogenèse et ge - Trächtigkeit die Länge des Fortpflanzungszyklus'. Die Gat- sta tion simultanées. Le requins des genres Carcharhinus, cer- tungen Rhizoprionodon, Mustelus und teilweise Sphyrna tains Sphyrna, et Ginglynostoma ont un cycle biennal avec haben einen einjährigen Fortpflanzungszyklus mit gleichzeit- vitellogenèse et gestation consécutives. Galeocerdo cuvier a iger Vitellogenese und Trächtigkeit und folglich einmal im une période de gestation de 12 mois, dans l’Atlantique Jahr Nachwuchs. Die Weibchen von Carcharias taurus haben ouest, et son cycle de reproduction peut être biennal. Car- offenbar einen zweijährigen Zyklus mit diskontinuierlicher charhinus obscurus a une période de gestation de 18 mois et Ovulation. Bei Alopias spp. ist der Zyklus einjährig bei zeit- probablement un cycle de reproduction de trois ans. Le cycle 205 aqua vol. 15 no. 4 - 15 October 2009 Observations on the reproductive cycles of some viviparous North American sharks biennal, avec toutes ses variations, se trouve chez des requins cycles are evident, and the purpose of this paper is de diverses origines phylétiques, comme les requins car- to present some of the evidence for these cycles that charhinoïdés, squaloïdés et orecto loboïdés, en accord avec I have observed in viviparous North American leurs processus physiologiques communs qui réclament un shark species. This paper is not a comprehensive long laps de temps pour accumuler l’énergie nécessaire à la production de leur progéniture. review of the reproductive cycles of sharks; it is a sketch of the cycles of some North American Sommario sharks, as it is certain that other patterns exist. Il ciclo riproduttivo degli squali è definito dalla frequenza Hopefully, this paper will stimulate others to con cui una specie dà origine a una prole e consta di due demonstrate other reproductive cycles. fasi: vitellogenesi e gestazione. Questi due periodi possono In a given shark population, the females can be essere simultanei o sequenziali e la durata di ognuno è va - reproductively synchronous or asynchronous. Syn- ria bile. Nell’insieme, vitellogenesi e gestazione determi- chronous females are in the same stage of the nano la lunghezza del ciclo riproduttivo. I generi Rhizopri- reproductive cycle, while in a population of asyn- onodon, Mustelus e alcune specie di Sphyrna hanno cicli annuali con vitellogenesi e gestazione contemporanee e chronous females, all can be at different stages of pertanto generano una prole all’anno. Le femmine di Car- the reproductive cycle. Generally, the females are charias taurus hanno in ciclo biennale con ovulazione dis- synchronous in species living in temperate waters, continua. Alopias spp. ha un ciclo annuale con vitellogene - where birth must occur at the most propitious time si e gestazione contemporanee e ha ovulazione continua. for the young to survive, generally in spring or Squalus acanthias ha un ciclo squaloide biennale con vitel- summer when temperatures are well within the logenesi e gestazione contemporanee. Gli squali dei generi thermal tolerances of the species and when prey or Carcharhinus, alcune specie di Sphyrna e Ginglymostoma food are abundant (Fig. 1). Females are often hanno un ciclo biennale con vitellogenesi e gestazione se - quenziali. Nell’Atlantico occidentale Galeocerdo cuvier ha reproductively asynchronous in species dwelling in un periodo di gestazione di 12 mesi e il ciclo riproduttivo tropical waters, where stable environmental condi- potrebbe essere biennale. Carcharhinus obscurus ha una tions and abundant food throughout the year per- gestazione di 18 mesi e probabilmente il ciclo riproduttivo mit reproduction and birth to occur year around ha una durata di tre anni. Il ciclo biennale, in tutte le sue (Fig. 2). varianti, è presente negli squali di diversa origine filetica When dealing with populations of synchronous come i carcarinoidi, gli squaloidi e gli orectoloboidi e females, the length of the gestation period can be riflette la loro comune fisiologia che richiede tempi lunghi calculated by following the development of the per accumulare sufficiente energia necessaria a dare origine a una prole. embryos throughout gestation. The length of the vitellogenesis period can be estimated by following the development of oocytes. The length of the INTRODUCTION reproductive cycle depends on the duration of The reproductive cycle of sharks can be defined vitellogenesis and of gestation, and whether the by how often a species breeds and consists of two two periods are concurrent or consecutive. Several periods. The first is the vitellogenesis period, when patterns result from the different possible combi- nutrients stored in the liver are transferred to the nations. Some of these patterns have a phyloge- developing oocytes in the ovary or ovaries, and netic basis. For example, squaloid sharks have bien- when oocytes accumulate yolk and grow rapidly. nial cycles with concurrent vitellogenesis and ges- The second is the gestation period, or the time of tation (see below), while sharks of the genus Car- embryonic development from fertilization to birth. charhinus generally have biennial cycles with con- Vitellogenesis and gestation can run concurrently secutive, year-long vitellogenesis and gestation or consecutively, and the duration of each period is (Castro 1993, 1996). variable. The duration of these periods depends on how effectively the mother can sequester energy MATERIALS AND METHODS from the environment and transfer it to the devel- Sharks were collected or examined from South

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