Spawning origins and ontogenetic movements for demersal fishes: An approach using eye-lens stable isotopes

Highlights

• Bulk isotope values in fish eye-lens cores provide a historical reference.

• Combined with external data sources, isotopes infer larval origin and movement.

• Four reef-associated fish species each display unique isotope patterns.

• Red Snapper are spawning on the West Florida Shelf.

• The technique can be applied to other shelf systems with strong isoscapes.

Abstract

The larval to postlarval period (the period between egg and juvenile) of many continental-shelf fish species lasts only a few weeks but has been shown to be critical to survival. During this period, individuals may travel long distances from spawning to juvenile habitats and are often difficult to locate. Fish eye lenses, which are constructed sequentially with minimal tissue turnover, record successive isotopic values for the entire lifespan. We present a widely applicable method of using the isotope values from the inner-most eye lens lamina (core: representing the larval to postlarval period) as a historical record of early life movement and location. By correlating the eye-lens core δ¹³C and δ¹⁵N values with juvenile capture location (i.e. settlement habitat) or with core size (i.e., growth during the first few weeks of life), we interpreted variability within the isotope values of a species as geographic origin and movement. We then evaluated the method using four northeastern Gulf of Mexico reef-fish species. Gag isotope values indicated movement inshore during the postlarval period. Red Grouper values suggested movement in both the inshore and alongshore directions. Black Seabass isotope values indicated a widely distributed early life with potential southward movement. Red Snapper isotope values suggested that larvae and postlarvae are widely distributed along the outer continental shelf, but do not move far from spawning origins in the eastern Gulf of Mexico. Bulk isotope values in fish eye lens cores can strengthen early life origin and movement data for many species of marine fishes, including those for which little early-life information exists.

Introduction

Many continental shelf fish species use disparate habitats throughout life (e.g., Kurth et al., 2019; Coleman and Williams, 2002; Hanson et al., 2013), with spawning occurring far from juvenile settlement locations (Saul et al., 2012; Weisberg et al., 2014; Tzadik et al., 2015). Whereas the larval to postlarval period (the period between egg and juvenile) lasts only weeks in most bony fishes, it can be critical in the survival of individuals and populations in many marine species (Houde, 2009). Because planktonic or semi-planktonic fish larvae can drift extensive distances, larval collections of coastal fish species are often spatially decoupled from both spawning and juvenile habitats (Colin, 2012; Burghart et al., 2014; Weisberg et al., 2014). Moreover, the larvae collected in ichthyoplankton surveys may not represent the proportion of the population that survives to the juvenile or adult stage (Burghart et al., 2014).

Bulk stable isotope values can be used as natural tags, providing information on geographic location (Seminoff et al., 2012; Trueman et al., 2017), movement (McMahon et al., 2011; MacKenzie et al., 2012), and trophic position (Post, 2002; Guinan et al., 2015; Dalponti et al., 2018). Many isotope-based investigations have focused on white muscle or other rapidly regenerating tissues (e.g. Brame et al., 2014; Haas et al., 2009; McMahon et al., 2013). Archival tissues such as otoliths (Dorval et al., 2007) and eye-lenses (Tzadik et al., 2017) have the potential to provide isotopic histories, including movement during the larval period (Nishida et al., 2020).

Fish eye lenses grow throughout life, sequentially adding thin layers of cells (laminae) to the outer margin of the lens (Nicol, 1989; Vihtelic, 2008). As lens size increases, the amount of protein required to cover the outside of the lens also increases. Because new lens cells experience minimal reworking after formation, the bulk isotopic composition of each eye-lens lamina reflects isotopic composition within the body during the time of lamina formation (Lynnerup et al., 2008; Nielsen et al., 2016). Thus, fish eye lenses sequentially preserve lifetime bulk stable isotope records (Wallace et al., 2014; Quaeck-Davies et al., 2018; Curtis et al., 2020) that can be reconstructed with an approximate frequency of two to three months (Wallace et al., 2014; Granneman, 2018). Some marine fishes, such as sharks and rays, rely on maternal nutrition for extended periods during early life, which is reflected in the isotope values of the eye-lens (Simpson et al., 2019). However, most marine bony fishes begin exogenous feeding within 72 h of hatching and at a total body length of only a few mm (Mullaney and Gale, 1996; Berlinsky et al., 2000; Drass et al., 2000; Lim and Mukai, 2014). Thus, the δ¹³C and δ¹⁵N values of the inner-most eye-lens material (hereafter, the eye-lens “core”) reflect the geographic location and diet (trophic position and basal-resource dependence) during the earliest weeks of life in these species (Wallace et al., 2014; Curtis et al., 2020).

The West Florida Shelf (WFS) in the northeastern Gulf of Mexico is a mosaic of soft- and hard-bottom habitats (Locker et al., 2010; Hine and Locker, 2011; Wall and Stallings, 2018) that extend over 600 km from north to south and over 200 km west from the Florida peninsula. Background isotope values and ranges in this region (Fig. 1a) remain remarkably stable among species, seasons, and years (Radabaugh et al., 2013; Huelster, 2015; Peebles and Hollander, 2020). The total range of background δ¹⁵N values for the region is approximately 4.4‰ (Fig. 1a) with variation in δ¹⁵N values likely driven by spatial variation in fluvial input and nitrogen fixation. Values of δ¹⁵N are highest toward the northwestern WFS and lowest to the southeast, coinciding with distance from large freshwater inflows that contribute terrestrial nitrogen to the north-central Gulf of Mexico (Radabaugh and Peebles, 2014; Peebles and Hollander, 2020). The total range of background δ¹³C values is approximately 3.6‰ (Fig. 1a). Trends in background δ¹³C values are roughly orthogonal to δ¹⁵N, with δ¹³C values highest close to shore and lowest close to the shelf edge. These trends are likely driven by photosynthetic fractionation, microalgal species composition, and/or changes in reliance on benthic or planktonic microalgae as basal resources (Radabaugh et al., 2014). Light environment, in particular, is thought to influence photosynthetic fractionation with shallow, clear water resulting in higher baseline δ¹³C values (less fractionation) than deep, less-clear waters (Fry and Wainright, 1991; Radabaugh et al., 2014). The primary trends in water depth and water clarity as well as location and relative volume of fluvial input tend to be stable on the WFS over time, resulting in stable background δ¹³C and δ¹⁵N values for the region.

Many commercially and recreationally valuable fish species use the WFS throughout their lifespans, yet the larval and postlarval periods remain largely unstudied in many species due to complex life histories, difficulty accessing specimens, and a large geographic region. Red Grouper (Epinephelus morio) inhabit low-relief, hard-bottom areas of the WFS, with juveniles occurring in shallower water than adults (Moe, 1969; Johnson and Collins, 1994; Lombardi-Carlson, 2014). This species has been observed spawning in small groups scattered across the WFS (Coleman et al., 1996, 2010), with the highest spawning activity recorded near the 70 m isobath (Wall et al., 2011; Grasty et al., 2019). Gag (Mycteroperca microlepis) spawn in large groups near the outer WFS (Fitzhugh et al., 2005; Ellis and Powers, 2012). Juvenile Gag subsequently inhabit the polyhaline regions of embayments for a year or more (Stallings et al., 2010; Switzer et al., 2012), and non-spawning adults use high-relief habitats in the shallow coastal zone (Bullock and Smith, 1991). Black Seabass (Centropristis striata) tend to be concentrated in low-relief, hard-bottom regions of the northern WFS (Hood et al., 1994; Weaver, 1996), with little data available to indicate whether ontogenetic habitat shifts occur. Red Snapper (Lutjanus campechanus) have recently re-expanded their range southeastward along the WFS after several years of strict harvest controls (Hollenbeck et al., 2015). Planktonic Red Snapper eggs have been genetically identified, and several females with hydrated oocytes have been captured on WFS reefs (Burrows et al., 2018; Nguyen, 2020), indicating spawning now occurs in the region. However, the distributions of spawning locations, eggs, and larvae on the WFS are unknown.

The objective of this study was to create a broadly applicable interpretation method for inferring fish early-life geographic origins and movement patterns using eye-lens stable isotope data. We used simultaneous correlation (Du et al., 2003; Zhang et al., 2006; Mahmoud and Sunarso, 2018) to evaluate the geographic origins and movements of demersal species from the northeastern Gulf of Mexico. Two of the species (Red Grouper and Gag) had well-known spawning and juvenile locations while these parameters were less well-understood in the other two (Red Snapper and Black Seabass). The current work represents a test case, but we designed the approach to be applicable to the study of any fish species in any region with consistent background isoscape trends.