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<I>Caranx Ignobilis</I>

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<I>Caranx Ignobilis</I> Bull Mar Sci. 97(2):257–280. 2021 research paper https://doi.org/10.5343/bms.2019.0114 Phylogeography of two marine predators, giant trevally (Caranx ignobilis) and bluefin trevally (Caranx melampygus), across the Indo-Pacific 1 Yale University, Department Jessica R Glass 1, 2 * of Ecology and Evolutionary Scott R Santos 3 Biology, PO Box 208106, New 4 Haven, Connecticut 06520 John SK Kauwe 4 2 South African Institute for Brandon D Pickett Aquatic Biodiversity, Private Thomas J Near 1, 5 Bag 1015, Grahamstown, South Africa 6140 3 Auburn University, Department of Biological Sciences, 101 Rouse ABSTRACT.—For economically valuable marine fishes, Life Science Building, Auburn, Alabama 36849 identifying biogeographic barriers and estimating the extent of gene flow are critical components of fisheries management. 4 Brigham Young University, We examined the population genetic structure of two Department of Biology, 4102 LSB, Provo, Utah 84602 commercially important reef-associated predators, the giant trevally (Caranx ignobilis) and bluefin trevally Caranx( 5 Yale Peabody Museum of melampygus). We sampled 225 individuals and 32,798 single Natural History, Division of nucleotide polymorphisms (SNPs) of C. ignobilis, and 74 Vertebrate Zoology, New Haven, Connecticut 06520 individuals and 43,299 SNPs of C. melampygus. Analyses of geographic population structure indicate the two species * Corresponding author email: display subtly different phylogeographic patterns. Caranx <[email protected]> ignobilis comprises two to three putative populations—one in the Central Pacific, one inhabiting the Western Pacific and Eastern Indian oceans, and one in the Western Indian Ocean—with some restricted gene flow between them. Caranx melampygus shows evidence of restricted gene flow from Hawaii to the West Pacific and Indian oceans, as well as limited genetic connectivity across the Indo- Pacific Barrier. Both species exhibit patterns characteristic of other large, reef-associated predators such as deepwater snappers and the great barracuda. This study contributes to ongoing assessments of the role of the Indo-Pacific Barrier in shaping patterns of phylogeography for large reef-associated fishes. Furthermore, by identifying putative populations of C. ignobilis and C. melampygus in the Central Pacific, our Handling Editor: John F Walter III findings serve to improve future management measures for these economically important, data-limited species, Date Submitted: 12 December, 2019. Date Accepted: 3 March, 2021. particularly in light of historic and contemporary overfishing Available Online: 3 March, 2021. in Hawaii. Understanding geographic patterns of genetic variation for economically impor- tant marine fishes is critical for determining stock structure, barriers to migration, patterns of recruitment, and other biological components necessary to manage the Bulletin of Marine Science 257 © 2021 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 258 Bulletin of Marine Science. Vol 97, No 2. 2021 exploitation of populations in a spatial context (Hellberg et al. 2002, Palumbi 2004, Bradbury et al. 2008). For example, the design of effective marine reserves relies on models of gene flow, spawning time and location, and physical and biological vari- ables of larval dispersal (Apostolaki et al. 2002, Sala et al. 2002, Palumbi 2003, Green et al. 2015). Gathering relevant biological data for transboundary fisheries manage- ment is of utmost importance, especially for predatory fishes, which are the most exploited in the world’s oceans (Pauly et al. 1998, Sibert et al. 2006, Fenner 2014). Tunas, swordfish, and other pelagic, predatory fishery species have received sig- nificant genetic research attention because of their high commercial value (Ward 1995, Lu et al. 2006, Jackson et al. 2014, Antoniou et al. 2017, Pecoraro et al. 2018). However, large knowledge gaps remain for species that are primarily harvested for artisanal and small-scale commercial fisheries (Salas et al. 2007, Jacquet and Pauly 2008, Pilling et al. 2009, Evans and Andrew 2011). Giant trevally (Caranx ignobilis) and bluefin trevally Caranx( melampygus; Fig. 1) are top-predator marine species (Glass et al. 2020) that are economically important for recreational, artisanal, and small-scale commercial fisheries across their ranges (Abdussamad et al. 2008, FAO 2014). They are frequently targeted by sportfishing charters in locations such as Hawaii, Japan, South Africa, Kenya, Indian Ocean is- lands (e.g., Seychelles, Maldives), as well as in the Red Sea and Gulf of Oman (Gaffeny 2000, Meyer et al. 2001, Maggs 2013, EAD 2014). The two species hold historical cultural significance for Native Hawaiians, but due to overharvesting and dangers to humans of ciguatera poisoning, the fishery for C. ignobilis and C. melampygus has been limited by state-mandated closures (Gaffeny 2000, Friedlander and Dalzell 2004, Nadon 2017). Both species share a distribution in tropical and subtropical wa- ters in the Indian and Western Pacific oceans, while C. melampygus is also resident in the Eastern Pacific, extending to the western coasts of Central and South America. Although C. ignobilis has a body size larger than that of C. melampygus—reach- ing up to 180 cm fork length (FL) compared to 117 cm FL—both species are often seen schooling together and have been reported to hybridize (Sudekum et al. 1991, Honebrink 2000, Murakami et al. 2007, Santos et al. 2011). Studies on the movement behavior of C. ignobilis indicate high adult residency, with daily vertical migrations and periodic to seasonal excursions of tens to hun- dreds of kilometers, presumably for feeding and spawning (Meyer et al. 2007, Lédée et al. 2015, Papastamatiou et al. 2015, Filous et al. 2017, Daly et al. 2019). To date, large spawning aggregations (>1000 individuals) of C. ignobilis have been identified in northern and southern Mozambique and the Philippines (von Westernhagen 1974, da Silva et al. 2015, Daly et al. 2018). While less studied than C. ignobilis, individu- als of C. melampygus in Hawaii exhibit similar movement behavior, specifically diel movement patterns and site fidelity (Holland et al. 1996, Meyer and Honebrink 2005, Filous et al. 2017). The extent to which both species travel to spawn seems depen- dent on geographic location as well as habitat and oceanographic features (Holland et al. 1996, Daly et al. 2019). Both species spawn in summer months, and multiple spawning events within a season have been reported (Sudekum et al. 1991, Meyer et al. 2007, Daly et al. 2018). Both C. ignobilis and C. melampygus associate with coral and rocky reefs, yet are sometimes also classified as semipelagic, similar to other large fishes such as barracudas Sphyraena( spp.) and yellowtail amberjacks (Seriola spp.; Gold and Richardson 1998, Babbucci et al. 2006, Daly-Engel et al. 2012). The widespread distributions of C. ignobilis and C. melampygus imply high dispersal Glass et al.: Phylogeography of giant and bluefin trevallies 259 Figure 1. (A) Giant trevally (Caranx ignobilis) and (B) bluefin trevally Caranx( melampygus) adults and juveniles. Illustrations by Elaine Heemstra, courtesy of the South African Institute for Aquatic Biodiversity. capacities, but the territorial behaviors and site-fidelity patterns observed in these two species convolute the expectations of long-distance connectivity. Because of their Indo-Pacific distributions, large body sizes, and life histories, characterizing the phylogeographic patterns of C. ignobilis and C. melampygus is relevant for ongoing work assessing the role and importance of major biogeographic barriers, such as the Indo-Pacific Barrier (IPB). The IPB, comprised of the Indonesian Archipelago, is a biogeographic barrier for marine organisms between the Indian and Pacific oceans (Briggs 2009), and much research has focused on how the IPB has facilitated and maintained high levels of species diversity in the Coral Triangle (Cowman and Bellwood 2013, Crandall et al. 2019). The Coral Triangle serves as both a biological diversity hotspot and a scientific hotspot for phylogeographic studies (Barber et al. 2011, Carpenter et al. 2011, Crandall et al. 2019). The extent to which patterns of gene flow and larval dispersal across the IPB are consistent among marine fishes and invertebrates remains an ongoing topic of research (Horne 2014, Keyse et al. 2014). Most studies have examined the influence of the IPB on shallow-water coral 260 Bulletin of Marine Science. Vol 97, No 2. 2021 reef fishes (Bowen et al. 2013, Keyse et al. 2014, Crandall et al. 2019), although re- search on deeper water and pelagic fishes has contributed to characterizing the com- plexity of the IPB (Reece et al. 2010, Gaither et al. 2011, Jackson et al. 2014). While the IPB serves as a barrier to population connectivity for many coral reef fishes (Bowen et al. 2016), other species exhibit gene flow across the IPB, facilitated by life history characteristics, directional flow, and magnitude of ocean currents (Carpenter et al. 2011, Horne 2014, Keyse et al. 2014, Crandall et al. 2019). Caranx ignobilis and C. melampygus are members of the clade Carangoidei (Girard et al. 2020), whose bulk of species diversity is located in the Coral Triangle. Some carangoid species (e.g., Seriola spp. and Trachurus spp.) have received substantial research attention due to their economic importance (Gold and Richardson 1998, Cárdenas et al. 2005, Purcell et al. 2015, Moreira et al. 2019). For many of these species, genetic
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