Lunar-induced reproductive patterns in transitional habitats: Insights from a Mediterranean killifish inhabiting northern Adriatic saltmarshes

Highlights

• The study aims to assess the reproductive cyclicity in Aphanius fasciatus.

• A semi-lunar periodicity was found both in reproductive behaviour and egg development.

• A. fasciatus reproduction appears to be adapted to saltmarsh dynamics.

Abstract

Estuaries and coastal lagoons play a key role in the functioning of coastal ecosystems and represent important natural areas for fish communities. Species living in these habitats often show specialised ecological and life history traits. The reproductive periodicity of a northern population of the Mediterranean killifish Aphanius fasciatus was assessed using the male courtship behaviour as indicator of reproductive motivation under laboratory conditions. Timing of egg development was also checked to further support the existence of a tidal-related periodicity. Using a statistical model applied to the intensity of courtship behaviour measured over a two-month period, a semilunar periodicity was revealed, with two main peaks corresponding with full moons. Both behaviours and timing of egg development were consistent with a periodicity of 14 days, suggesting that the tidal cycle drives the reproduction of A. fasciatus in Northern Adriatic saltmarshes. The findings are assessed with a comparative approach within both European and North American transitional waters.

Introduction

A large number of fish species exhibit lunar-related reproductive patterns (Takemura et al., 2004). Within this wide spectrum of cases, lunar phases can either trigger reproductive synchronisation, as shown for example in many coral reef fishes (Robertson et al., 1990, Robertson, 1991, Takemura et al., 2004), or couple tidal peaks with reproduction in intertidal environments (Taylor, 1999). According to Taylor (1999), adults of many aquatic species living in the intertidal zone show a typical reproductive periodicity that allows sexual maturity and egg hatching to occur when the intertidal zone is under most complete immersion thus maximising individual reproductive success. Saltmarshes are highly valuable habitats in both North American and European transitional water bodies, as they host many animal species of both conservation and commercial interest, thus providing ecosystem services to humans, such as biological resources from fisheries, recreational activities and tourism (Hampel et al., 2003, Franco et al., 2006b, Franzoi et al., 2010). Although the typical European saltmarsh is situated higher in the intertidal zone than in the US (Hampel et al., 2003), in both continents the use of these habitats by aquatic and terrestrial organisms is expected to be periodic and cyclic. For intertidal spawners, the most commonly used study models include some Teleost fish species. For intertidal reproducers, the most commonly used study models include some Teleost fish and among them, killifishes of the genus Fundulus have been extensively studied, showing reproductive periodicity under both laboratory and field conditions (Taylor, 1999). The most common feature emerging from these studies is the presence of a semilunar pattern of spawning, involving the cycles of both ovarian follicles and egg deposition and hatching (Greeley et al., 1986, Hsiao et al., 1994, Hsiao et al., 1996; Cerdá et al., 1996). Despite this common pattern, longitudinal variability in this reproductive periodicity has been shown within Fundulus species or between sub-species, indicating that this tidal-dependent reproductive cycle may vary across local populations, as a response to other environmental or genetic factors (McMullin et al., 2009, Petersen et al., 2010). Within the Mediterranean area, the ecological equivalent of the genus Fundulus is probably represented by the genus Aphanius. Many studies have been conducted on the most abundant species of this genus, the South European Toothcarp Aphanius fasciatus (Valenciennes, 1821) (Maltagliati, 1998, Maltagliati, 1999, Maltagliati, 2002, Maltagliati et al., 2003, Ferrito et al., 2003, Ferrito et al., 2007), mainly addressing genetic and morphological traits of populations. This fish belongs to the family Cyprinodontidae, being therefore not phylogenetically too distant from Fundulidae. Furthermore, in the northern part of its geographic range, and namely within the Northern Adriatic lagoons, this fish is one of the most abundant and recurrent fish species in saltmarsh habitats, where it spends the entire life cycle (Franco et al., 2006b, Franzoi et al., 2010, Cavraro et al., 2011). In this area, saltmarshes are subjected to one of the highest tidal excursions of the entire Mediterranean Sea. These environments are characterised by a complex systems of creeks and pools of different size, which are rich in both riparian and submerged aquatic vegetation. Although field studies on the reproductive behaviour of this species are lacking in the literature, laboratory and field observations (Cavraro et al., 2014; Leonardos, personal observation) suggest that saltmarshes are used for reproduction. The eggs of this species are attached by the female to the vegetation through a system of adhesive filaments (chorion filaments, similarly that which happens in Fundulidae), after being conducted by males to the adequate substratum by means of an elaborated courtship. Furthermore, fry are found in small shallow pools within these marsh systems (Cavraro et al., 2014). These observations suggest that reproduction occurs within these habitats and reproductive patterns should therefore synchronise with the phases of maximum water inflow.

The present study aimed to assess the lunar-related reproductive periodicity of Venice lagoon populations of Aphanius fasciatus under laboratory conditions. In addition, egg development was obtained under aquarium conditions, to assess time of development and hatching, in order to further support the existence of an intertidal adaptation in this species. The two main questions addressed here are: 1) is the reproductive cycle of A. fasciatus lunar-related? 2) is the timing of egg development consistent with a tidal/lunar cycle? Results are then discussed comparing the present Aphanius model with the well-known Northern American Fundulus model.