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Patterns in Micronekton Diversity Across the North Pacific Subtropical Gyre Observed from the Diet of Longnose Lancetfish (Alepisaurus Ferox)

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Patterns in Micronekton Diversity Across the North Pacific Subtropical Gyre Observed from the Diet of Longnose Lancetfish (Alepisaurus Ferox) Author’s Accepted Manuscript Patterns in micronekton diversity across the North Pacific Subtropical Gyre observed from the diet of longnose lancetfish (Alepisaurus ferox) Elan J. Portner, Jeffrey J. Polovina, C. Anela Choy www.elsevier.com PII: S0967-0637(16)30357-0 DOI: http://dx.doi.org/10.1016/j.dsr.2017.04.013 Reference: DSRI2784 To appear in: Deep-Sea Research Part I Received date: 28 October 2016 Revised date: 7 March 2017 Accepted date: 18 April 2017 Cite this article as: Elan J. Portner, Jeffrey J. Polovina and C. Anela Choy, Patterns in micronekton diversity across the North Pacific Subtropical Gyre observed from the diet of longnose lancetfish (Alepisaurus ferox) , Deep-Sea Research Part I, http://dx.doi.org/10.1016/j.dsr.2017.04.013 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Patterns in micronekton diversity across the North Pacific Subtropical Gyre observed from the diet of longnose lancetfish (Alepisaurus ferox) Elan J. Portnera*, Jeffrey J. Polovinab, C. Anela Choyc aHopkins Marine Station, Stanford University, 120 Ocean View Blvd., Pacific Grove, CA 93950, USA bNOAA Pacific Islands Fisheries Science Center 1845 Wasp Blvd., Honolulu, HI 96818, USA cMonterey Bay Aquarium Research Institute 7700 Sandholdt Road, Moss Landing, CA 95039, USA [email protected] [email protected] [email protected] *Corresponding author Abstract: We examined the diet of a common midwater predator, the longnose lancetfish (Alepisaurus ferox, n= 1371), with respect to fork length, season, and capture location within the North Pacific Subtropical Gyre (NPSG). While A. ferox fed diversely across 98 prey families, approximately 70% of its diet by wet weight was contributed by seven prey families (fishes: Sternoptychidae, Anoplogastridae, Omosudidae, Alepisauridae; hyperiid amphipods: Phrosinidae; octopods: Amphitretidae; polychaetes: Alciopidae). Altogether, these micronekton prey families constitute a poorly known forage community distinct from those exploited by other pelagic predators and poorly sampled by conventional methods. We demonstrate ontogenetic variation in diet of A. ferox between two size classes of a bimodal size structure of our specimens (<97cm fork length = “small”, ≥97cm fork length = “large”). Large A. ferox consumed more fish and octopods, fewer crustaceans, and were more cannibalistic than small A. ferox. Multiple observations supported ontogenetic shifts in vertical foraging habitat, including that large A. ferox consume more mesopelagic and larger prey overall, than small A. ferox. Spatial and 1 seasonal variation in the diet of A. ferox is consistent with expected patterns of variation in prey distribution with respect to oceanographic features of the NPSG. Within both size classes, the diets of specimens collected from the oligotrophic core of the NPSG were more diverse than those collected near the boundaries of the gyre and appeared to track seasonal variation in the position of the northern boundary of the gyre. Our data suggest seasonal and spatial variability in the midwater forage communities exploited by A. ferox across the NPSG, and demonstrate that sustained monitoring of diet would provide valuable insights into the long-term changes in these understudied communities. Keywords – Pelagic ecology, trophic dynamics, mesopelagic predator, diet analysis, biological sampler, lancetfish, micronekton, North Pacific Subtropical Gyre 1. Introduction Pelagic ecosystems are the largest on the planet in terms of volume (Ramirez-Llodra et al., 2010; Robison 2009) and support numerous species which are commercially harvested (e.g. tunas, billfishes, sharks, and squids; FAO 2012) or protected (e.g. whales, dolphins, and birds; Moore et al., 2009). Many of these species are direct predators of micronekton – actively swimming fishes, crustaceans, cephalopods, and gelatinous organisms approximately 2-20cm in length, which comprise a large biomass in pelagic ecosystems and link production at the base of the food web to top predators (Brodeur & Yamamura, 2005; Dambacher et al., 2010; Moteki, et al., 2001). The composition of micronekton communities varies between ocean basins (Brodeur and Yamamura, 2005), and diel migration of many micronekton species between the surface and mesopelagic depths (~200-1000m) creates vertical variability in within ocean basins (Maas et al., 2014; Tont 1976; Young 1978). Although spatial and temporal variation in micronekton communities has been detected at the scale of ocean basins, there have been few community- scale studies of micronekton ( Maynard et al., 1975; De Forest and Drazen, 2009; Drazen et al., 2011) and many species are able to actively avoid trawls, limiting our ability to thoroughly sample these dynamic midtrophic communities with conventional methods (Clarke, 1973; Kaartvedt et al., 2012). As such, natural variation in micronekton communities and their 2 responses to perturbations represent a critical gap in our understanding of pelagic ecosystem dynamics (Lehodey et al., 2010; Young et al., 2015). For pelagic fish predators, diet analysis is commonly used to study vertical distributions (Choy et al., 2013; Moteki, et al., 2001), variability in trophic ecology over space and time (Kuhnert et al., 2012; Olson and Galván-Magaña, 2002; Watanabe et al., 2009), and has been used in concert with acoustic and trawl surveys to assess temporal variability in prey availability and selectivity (Bertrand et al., 2002). Examining prey communities through diet is inherently biased by foraging behaviors, but provides access to prey that escape capture by midwater trawls. In the case of mesopelagic predators, diet analysis augments our understanding of deep-dwelling communities difficult to sample at high spatial or temporal resolutions. Previous work has shown that large pelagic fish can serve as biological samplers of micronekton and diet analysis can be used to detect large-scale changes in pelagic food webs (Olson et al., 2014; Overholtz et al., 2000). Most of the effort to elucidate pelagic trophic dynamics has been focused on commercially important apex predators, such as tunas and billfishes, many of which are metabolically tied to warm waters at the ocean’s surface (Block et al., 1992, 1997; Dewar et al., 2011, Olson et al., 2016). Examining the trophic ecology of deeper-dwelling, midtrophic predators could greatly augment our understanding of variability in the structure of mesopelagic micronekton communities by increasing the diversity of forage communities sampled. The longnose lancetfish, Alepisaurus ferox, is a midtrophic, mesopelagic predator found circumglobally at tropical and subtropical latitudes (Orlov & Ul’chenko, 2002), and is known mostly from reports of incidental catch in tuna and swordfish longline fisheries (Carruthers et al., 2009; Jantz et al., 2013; Uchiyama et al., 2003) and onshore records of dead individuals (Kubota & Uyeno, 1970; Orlov & Ul’chenko, 2002). Very little is known about the growth rate or life history of A. ferox; its maximum reported length is 215cm (Robins & Ray, 1986) and exploratory histological studies suggest that A. ferox is a simultaneous hermaphrodite, although the functionality of each gonad throughout its life history is unknown (Gibbs 1960, Smith & Atz, 1973). Alepisaurus ferox has a large, blind-sac gut typical of fishes in the suborder Alepisauroidea, but appears to store food in its stomach for extended periods with minimal digestion (Wassersug & Johnson, 1976), allowing for detailed prey identification. Diet studies from multiple ocean basins demonstrate that A. ferox consumes diverse prey (e.g. fishes, crustaceans, cephalopods, etc.) and have generally classified A. ferox as an opportunistic predator 3 (Moteki et al., 1993; Potier et al., 2007a, 2007b; Romanov et al., 2008). However, A. ferox from different locations have comparable diets (Choy et al., 2013, Romanov et al., 2008), suggesting that a better understanding of diet selectivity by A. ferox and the trophic niche it occupies will require more spatially expansive diet studies. Alepisaurus ferox plays important roles in pelagic ecosystems as both predator and prey (Moteki, et al., 2001; Potier et al., 2007a; Young et al., 2010). In the south- and central-western Pacific Ocean, A. ferox has been identified as a “key player” based on high numbers of trophic linkages and the negative modeled effects of its removal from these ecosystems (Dambacher et al., 2010). Within the North Pacific Subtropical Gyre (NPSG), which lies between 20º and 35º N latitude (Howell et al., 2012), the prevalence of A. ferox has increased over the past two decades in parallel with the expansion of the oligotrophic core of the NPSG (Polovina et al., 2008, 2011) and large-scale changes in the size structure and abundance of primary producers and top predators (Polovina et al., 2009; Barnes et al., 2011; Woodworth-Jefcoats et al., 2013). Fisheries observer data show that A. ferox was the most commonly captured species in the Hawaii-based, deep-set longline fishery between 2005 and 2015, but it is unclear how these trends relate to competitive release, reduction
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