Feeding Ecology of Early Life Stages of Mesopelagic Fishes in the 2 Equatorial and Tropical Atlantic 3 4 Tabit Contreras1*, M
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1 Feeding ecology of early life stages of mesopelagic fishes in the 2 equatorial and tropical Atlantic 3 4 Tabit Contreras1*, M. Pilar Olivar1, P. Alexander Hulley2,3, M. Luz Fernández de 5 Puelles4 6 7 1Institut de Ciències del Mar (CSIC), Passeig Marítim, 37-49, Barcelona 08003, Spain 8 2Iziko – South African Museum, Cape Town, South Africa 9 3MA-RE Institute, University of Cape Town, South Africa 10 4 Centro Oceanográfico de Baleares, Instituto Español de Oceanografía, Muelle de 11 Poniente s/n, 07015 Palma de Mallorca, Spain 12 13 14 *Corresponding author: tel: +34 932309500; fax: +34 932309555; e-mail: 15 [email protected] 16 17 18 19 20 21 22 23 24 25 26 27 28 1 29 Abstract 30 We analysed the trophic ecology of the early ontogenetic stages of six mesopelagic fish 31 species (Bathylagoides argyrogaster, Argyropelecus sladeni, Sternoptyx diaphana, 32 Diaphus vanhoeffeni, Hygophum macrochir, and Myctophum affine), which have 33 different morphologies, vertical distributions and taxonomic affiliations. The larvae and 34 transforming stages of the sternoptychids fed both during the day and at night. 35 However, larvae of the other species fed during the day, as they apparently rely on light 36 for prey capture. The transforming stages of myctophids showed a similar daylight 37 feeding pattern to their larvae, but in D. vanhoeffeni both day and night feeding was 38 evident, thereby indicating the progressive change towards the adult nocturnal feeding 39 pattern. The number of prey and their maximum sizes were linked to predator gut 40 morphology and gape size. Although the maximum prey size increased with predator 41 development, postflexion larvae and transforming stages also preyed on small items, so 42 that the trophic niche breath did not show evidence of specialization. In all the species, 43 copepods dominated the larval diet, but the transforming stages were characterized by 44 increasing diet diversity. Despite the poor development of these early stages, Chesson’s 45 selectivity index calculated for larvae and transforming stages showed positive selection 46 for particular prey. 47 48 Key words: Diet, selectivity, fish larvae, transforming stages, bathylagids, 49 hatchetfishes, myctophids. 50 51 2 52 Introduction 53 The mesopelagic zone is generally considered to lie between 200 and 1000 m depth in 54 the water column, although these values may vary slightly in different parts of the 55 World Ocean (Reygondeau et al., 2017), and is characterized by low light conditions. 56 Mesopelagic fishes are one of the most common components in open ocean samples 57 (Gjøsaeter and Kawaguchi, 1980; McGinnis, 1982). Their larvae have also been 58 reported as being the most abundant in ichthyoplankton samples (Moser and Ahlstrom, 59 1970, 1996). The fishes inhabiting this zone belong to taxa from the Orders 60 Myctophiformes, Stomiiformes, Anguilliformes, Argentiniformes, Aulopiformes, 61 Lophiiformes and Stephanoberyciformes (Weitzman, 1997). Although all these groups 62 may co-exist at a particular depth in the water column during the day, differential diel 63 vertical migratory behaviours have been reported for most myctophid species, and for 64 certain stomiiforms (families Phosichthyidae and Stomiidae) (Merrett and Roe, 1974; 65 Baird, 1971; Hulley, 1984; Olivar et al., 2017). The migratory fishes follow the nightly 66 zooplankton migration, ascending into the epipelagic layers to feed, and descending to 67 mesopelagic layers during the day to avoid predators and to digest their food (Baird et 68 al., 1975; Hopkins and Baird, 1985; Gartner et al., 1997; Mehner and Kasprzak, 2011; 69 Sutton, 2013; Bernal et al., 2013, 2015). While the adult fishes may have wide ranges in 70 their vertical distributions, their larval stages demonstrate a more limited vertical depth 71 range, mainly between the surface and 200 m. They only perform very restricted 72 vertical displacements, and therefore feed mainly in the upper water layers (Loeb, 1979; 73 Sabatés, 2004; Sassa and Kawaguchi, 2004, Sassa et al., 2007; Olivar et al., 2014, 74 2018). 75 Feeding ecology and the diets of mesopelagic fishes, based on stomach content 76 analyses, have been mainly investigated for the adult stages, and particularly in 77 myctophids (Clarke, 1980; Kinzer and Schulz, 1985; Hopkins and Gartner, 1992; Rissik 78 and Suthers, 2000; Watanabe et al., 2002; Bernal et al., 2013, 2015; McClain-Count et 79 al., 2017) and in stomiiform species (Sutton and Hopkins, 1996; Champalbert et al., 80 2008; Carmo et al., 2015; McClain-Counts et al., 2017). These fishes are mostly 81 opportunistic zooplankton feeders, but the diets of some species also include particulate 82 organic matter and small fish (Palma, 1990; Hopkins and Gartner, 1992; Watanabe and 83 Kawaguchi, 2003; Bernal et al., 2015). Knowledge of larval feeding is limited to fewer 84 species (e.g., Sabatés and Saiz, 2000; Conley and Hopkins, 2004; Sassa and Kawaguchi, 3 85 2004; Bernal et al., 2013; Contreras et al., 2015, for myctophids; and Palma, 1990; 86 Landaeta et al., 2011 for stomiiforms). Information on feeding in transforming stages is 87 even more scarce (Contreras et al., 2015). These studies have reported that the larvae of 88 mesopelagic fishes appear to feed on small zooplankton items, and that their diets are 89 related both to availability of prey and to larval development. While prey size is one of 90 the most important factors influencing prey capture, other factors can influence prey 91 capture, such as prey abundance, prey colour and the swimming behaviour of prey, so 92 indicating that fish larvae might not feed at random but may have selective capacity 93 (Hunter, 1981; Govoni et al., 1986; Llopiz, 2013; Robert et al., 2014). Among those 94 larval features related to feeding, the main constraints are gape size, swimming skill and 95 the development of sensory organs, in addition to larval behaviour itself (Hubbs and 96 Blaxter, 1986; Browman and O'Brien, 1992). The main environmental factor 97 influencing larval feeding is the light condition, because most fish larvae are visual 98 feeders (Blaxter, 1986; Huse, 1994). 99 Information on the distribution and abundance of mesopelagic fishes in the equatorial 100 and tropical Atlantic is relatively common (Hulley, 1981; Hulley and Krefft, 1985; 101 Hulley and Paxton, 2016a, b; Olivar et al., 2017). Investigations on their larval stages 102 have been focused in regions close to the continents (e.g., Badcock and Merrett, 1976; 103 Moyano et al., 2014; Olivar et al., 2016; de Castro et al., 2010; Bonecker et al., 2012; 104 Namiki et al., 2017), but recent research by Olivar et al., (2018) has analysed the overall 105 distribution and abundance patterns across the Atlantic, showing that larvae of 106 mesopelagic fishes dominate the first 100 m of the water column everywhere. 107 For the present investigation, we analysed the trophic ecology of larval and 108 transforming stages in six mesopelagic species with different larval morphologies, and 109 different vertical distributions: Bathylagoides argyrogaster (Bathylagidae), 110 Argyropelecus sladeni and Sternoptyx diaphana (Sternoptychidae), Diaphus cf. 111 vanhoeffeni, Hygophum macrochir and Myctophum affine (Myctophidae). Knowledge 112 of the feeding behaviour of the larvae of these species is lacking, and only feeding data 113 on the juvenile stages of A. sladeni and S diaphana have been published (Hopkins and 114 Baird, 1973). The present study compares feeding incidence, size spectra, trophic niche 115 breadth and diet composition, to determine if the larvae and transforming stages of the 116 six species have specific feeding patterns which can be correlated with their ontogenetic 117 development, vertical distribution and morphology. 4 118 Materials and methods 119 Sampling 120 In order to characterize the mesopelagic fauna and its environment, a survey comprising 121 a transect of 12 stations was undertaken during April 2015 across the tropical and 122 equatorial Atlantic on board Research Vessel Hesperides (82 m x 15 m). The cruise 123 extended from near the Brazilian coast to south of the Canary Islands, regions where 124 bottom depths range from 3000 to 5200 m (Figure 1) (Olivar et al., 2017, 2018). Fish 125 larvae were collected at 11 stations from 8 to 28 of April. Both day and night plankton 126 samples were obtained at each station within a 24-hour period. At each station, oblique 127 tows were undertaken using a MOCNESS-1 net (mouth opening of 1 m2), fitted with 8 128 nets of 200 μm mesh-size. Samples were taken in the following depth strata: 800-600 m, 129 600-500 m, 500-400 m, 400-300 m, 300-200 m, the lower thermocline layer (ca 200- 130 100 m), thermocline (ca. 50-100), and the upper mixed layer (ca. 50-0 m). During 131 trawling, the ship’s speed was maintained at 1.5-2.5 knots, and the winch retrieval rate 132 was 20 m/min. The total duration of each haul ranged from 5 to 10 min, except for the 133 deepest layer in which the mean duration was 24 min. The mean volume of water 134 sampled per layer was 470.8 m3 (SD 236.6), ranging between ca. 300 m3 (the shallowest 135 layer) to 870 m3 (the deepest and broadest layer), and with fairly similar volume vs time 136 ratios between layers (mean 50.7; SD 6.7 m3/min). 137 In addition to the mesozooplankton samples obtained with the MOCNESS-1 net, 138 microzooplankton samples were collected by vertical hauls with a Calvet net (0.25 m 139 diameter and 0.53 μm mesh-size), between 200 m and the surface. Zooplankton samples 140 were preserved in 5 % buffered formalin and kept in the dark until later investigation at 141 the laboratory. 142 Laboratory analysis 143 All fishes were sorted and identified to the lowest possible taxon.