Rev Iss Web Mec 13823 25-20 5203..5211

UC Santa Cruz UC Santa Cruz Previously Published Works Title Spatial patterns of self-recruitment of a coral reef fish in relation to island-scale retention mechanisms. Permalink https://escholarship.org/uc/item/3009m2hq Journal Molecular ecology, 25(20) ISSN 0962-1083 Authors Beldade, Ricardo Holbrook, Sally J Schmitt, Russell J et al. Publication Date 2016-10-01 DOI 10.1111/mec.13823 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Molecular Ecology (2016) 25, 5203–5211 doi: 10.1111/mec.13823 Spatial patterns of self-recruitment of a coral reef fish in relation to island-scale retention mechanisms RICARDO BELDADE,*†‡ SALLY J. HOLBROOK,§ RUSSELL J. SCHMITT,§ SERGE PLANES*† and GIACOMO BERNARDI¶ *EPHE, PSL Research University, UPVD, CNRS, USR 3278 CRIOBE, BP 1013, 98729, Papetoai, Moorea, French Polynesia, †Laboratoire d’excellence “CORAIL”, EPHE, PSL Research University, UPVD, CNRS, USR 3278 CRIOBE, BP 1013, 98729, Papetoai, Moorea, French Polynesia, ‡MARE – Marine and Environmental Sciences Centre, Faculdade de Ciências da, Universidade de Lisboa, Campo Grande, Lisboa 1749-016, Portugal, §Coastal Research Center, Department of Ecology, Evolution and Marine Biology, Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA 93106, USA, ¶Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95060, USA Abstract Oceanographic features influence the transport and delivery of marine larvae, and physical retention mechanisms, such as eddies, can enhance self-recruitment (i.e. the return of larvae to their natal population). Knowledge of exact locations of hatching (origin) and settlement (arrival) of larvae of reef animals provides a means to compare observed patterns of self-recruitment ‘connectivity’ with those expected from water circulation patterns. Using parentage inference based on multiple sampling years in Moorea, French Polynesia, we describe spatial and temporal variation in self-recruitment of the anemonefish Amphiprion chrysopterus, evaluate the consistency of net dispersal distances of self-recruits against the null expectation of passive particle dispersal and test the hypothesis that larvae originating in certain reef habitats (lagoons and passes) would be retained and thus more likely to self-recruit than those originating on the outer (fore) reef. Estimates of known self-recruitment were consis- tent across the sampling years (~25–27% of sampled recruits). For most (88%) of these self-recruits, the net distance between hatching and settlement locations was within the maximum dispersal distance expected for a neutrally buoyant passive particle based on the longest duration of the larval dispersive phase and the average direction and speed of current flow around Moorea. Furthermore, a parent of a given body size on the outer (fore) reef of Moorea was less likely to produce self-recruits than those in passes. Our findings show that even a simple dispersal model based on net average flow and direction of alongshore currents can provide insight into landscape-scale retention patterns of reef fishes. Keywords: connectivity, coral reef fish, oceanography, parentage analysis, retention, self- recruitment, tropical island Received 19 May 2016; revision received 11 August 2016; accepted 22 August 2016 populations are connected primarily via dispersal of lar- Introduction vae. Attributes of dispersal and settlement of marine Knowledge of animal and plant dispersal is fundamen- larvae can be influenced by the oceanographic condi- tal for understanding both the dynamics of populations tions they experience (Schmitt & Holbrook 2002; Cowen and evolution of species (Clobert et al. 2001; Ronce et al. 2007; Pineda et al. 2007) and their behaviour (Sto- 2007). For most marine reef fish, spatially separated butzki & Bellwood 1997; Kingsford et al. 2002; Paris & Cowan 2004; Paris et al. 2007). Generally, the probability Correspondence: Ricardo Beldade, Fax: +351217500009; E-mail: of successful larval dispersal diminishes with distance [email protected] from the hatching site (Pinsky et al. 2010; Buston et al. © 2016 John Wiley & Sons Ltd 5204 R. BELDADE ET AL. 2012), and a growing number of studies have shown water flows on the leeward side of tropical islands that net dispersal distances (shortest in-water distance (Swearer et al. 1999), may also favour the retention of between hatching and settlement sites) of successful fish larvae and thus influence dispersal. However, there is settlers can be short (~1 km scale). Examples of coral limited empirical support that spatial patterns of self- reef fishes that have displayed such short dispersal dis- recruitment for reef fishes are influenced by physical tances include Chaetodon vagabundus, Amphiprion percula, retention features. Given impracticalities in following A. polymnus, Plectropomus maculatus, Stegastes partitus, individual larvae throughout their entire pelagic disper- and Elacatinus lori (Almany et al. 2007; Buston et al. sal stages (Leis 1991), one approach to this issue has 2012; Harrison et al. 2012; Hogan et al. 2012; Saenz-Agu- been to use parentage inference to identify larvae that delo et al. 2012; D’Aloia et al. 2015), while others have recruit into their population of origin (e.g. Jones et al. been shown to disperse over much larger distances 2005; Almany et al. 2007; Beldade et al. 2012) and to (Planes et al. 2009; Berumen et al. 2012; Puebla et al. map the precise locations of hatching (origin) and of 2012; Simpson et al. 2014). settlement (arrival) of individual self-recruiting larvae. A long-standing issue has been the extent to which In this study, we first describe spatial and temporal locally vs. externally produced larvae replenish local variation in self-recruitment of a coral reef fish (the populations of reef organisms, with estimates of self- orange-fin anemonefish, Amphiprion chrysopterus), on recruitment varying from none to the majority of colo- Moorea, French Polynesia, over 5 years. Here, we define nists for reef fishes (D’Aloia et al. 2015; Steinberg et al. a self-recruit as a post-settlement juvenile on Moorea 2016). While high numbers of self-recruits need not that was produced by an adult on the island, and ‘self- imply that a high proportion of the locally produced recruitment connectivity’ as the spatial topology larvae have been retained (Botsford et al. 2009; Berumen between locations of origin and subsequent settlement et al. 2012; Burgess et al. 2014; Lett et al. 2015), the of self-recruits around Moorea. This enabled us to eval- degree of self-replenishment of populations has vast uate the consistency of putative dispersal trajectories of ecological and management implications. The retention self-recruits to a minimalistic passive particle dispersal of the dispersive stages of fish near suitable habitats model to assess how much of the connectivity in self- can both occur actively due to larval behaviours and recruitment could be accounted for by a simple physical passively through transport promoted by water move- transport model. Moreover, considering water flow pat- ment patterns (Paris & Cowan 2004). Coral reef fish lar- terns, we tested the hypothesis that larvae originating vae have a suite of sensorial and swimming abilities in different reef habitats (lagoon, pass, fore reef), which that steer them during the dispersal phase towards their implies being more or less exposed to certain water cir- settlement habitats. For example, hearing and smell culation regimes, vary in the degree of self-recruitment. have been shown to guide reef fish larvae during dis- Finally, we explore whether self-recruits and exogenous persal (Kingsford et al. 2002; Simpson et al. 2005; Ger- recruits (i.e. not produced by adults on Moorea) differ lach et al. 2007). Larvae from the same cohort can use in the reef habitats to which they settle. behaviour to remain together while dispersing (Paris & Cowan 2004), which can result in them settling concur- Methods rently to the same microhabitat (Bernardi et al. 2012). While fish larvae can use behaviours to enhance reten- Study site and model species tion (Paris et al. 2007), several water circulation features also can act to retain larvae, which may lend insight Field work was conducted on Moorea (17°300S, into spatial patterns of self-recruitment (Swearer et al. 149°500W), French Polynesia. The island is encircled by 1999). a barrier reef that forms a system of lagoons that are For islands encircled by a barrier reef, breaking 0.8–1.3 km wide and 5–7 m deep and are connected to waves create more or less a unidirectional flow of water the ocean by several passes. The offshore reef slopes over the reef crest into the lagoon, which later returns steeply to >500 m depth within about 1 km of the reef to the open ocean through one or more passes (open- crest. Several aspects of Moorea’s water circulation that ings in the reef) (Hench et al. 2008; Edmunds et al. 2010; are pertinent to transport and retention of larvae have Leichter et al. 2013). At smaller scales, within the been described in Leichter et al. (2013). An alongshore lagoon, varying degrees of turbulent mixing are forced flow just offshore of the barrier reef follows a net coun- by different coral species/morphologies (Monismith terclockwise direction (CCW) that may contribute to the 2007; Hench & Rosman 2013); longer water residence retention of larvae near the island (Leichter et al. 2013). time also could contribute to the retention

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