Spawning origins and ontogenetic movements for demersal fishes: An approach using eye-lens stable isotopes
Graphical abstract
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.
Section snippets
Specimen collection
We obtained juvenile Black Seabass (n = 51), Gag (n = 51), Red Grouper (n = 52), and Red Snapper (n = 38) from the fisheries-independent monitoring efforts of the Florida Fish and Wildlife Conservation Commission and the Southeast Area Monitoring and Assessment Program (SEAMAP). Between 2015 and 2017, specimens were collected from the WFS and from the mouths of embayments on the west coast of Florida (Fig. 1b). We measured each fish for standard length (SL). We extracted both eyes, wrapped them
Results
Age at collection ranged from under one year to over three years, and collection length ranged from 37 to 325 mm SL. Based on species-specific regressions between ELD and SL, the analyzed fish were in the range of 14–47 mm SL at the time of outer core formation, ranging from a few days pre-settlement (postlarval) to a few weeks post-settlement (early juvenile: Table 1). Mean values of both δ13C and δ15N were highest for Black Seabass with wide ranges in both. Red Snapper produced the largest
Discussion
We devised a novel strategy for inferring fish spawning distribution and early-life movement using δ13C and δ15N values from eye-lens cores, using known capture locations to aid interpretation. We evaluated the approach using four reef-associated fish species common to hard-bottom habitats of the WFS and found differences in both apparent spawning origin and apparent ontogenetic movement among species. Each species exhibited a unique distribution in both δ13C and δ15N values, suggesting
Conclusions and future directions
We show that isotope values within eye-lens cores, combined with juvenile catch location and ELD, yield inferences about spawning location and early life movement that are both consistent with known patterns and are broadly generalizable to populations with less biological information. Differences in the isotopic value central tendencies agreed with known or suspected differences in relative spawning locations and early-life habitat use (Coleman et al., 1996; Weaver, 1996; Saul et al., 2013).
Funding
Funding for this research was provided by University of South Florida College of Marine Science endowed fellowships and the Spawning Habitat and Early-Life Linkages to Fisheries (SHELF) project of the Florida RESTORE Act Centers of Excellence Program (FLRACEP), administered by the Florida Institute of Oceanography under awards 4710112604 and 4710112901 to the University of South Florida. These funding sources had no role in the study design, in the collection, analysis and interpretation of
CRediT authorship contribution statement
Julie L. Vecchio: Conceptualization, Data curation, Methodology, Project administration, Visualization, Writing - original draft, Writing - review & editing. Ernst B. Peebles: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Supervision, Visualization, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that influenced the work.
Acknowledgements
We thank Florida Fish & Wildlife Conservation Commission's Fisheries Independent Monitoring program and SEAMAP groundfish trawl survey for specimen collections. We thank members of the Peebles lab, especially Catie Bruger, Jennifer Granneman, Brianna Michaud, and Amy Wallace for assistance with dissections and eye-lens preparation. We also thank Ethan Goddard and the USF College of Marine Science Marine Environmental Chemistry Laboratory for isotope analysis. We thank the Fish and Wildlife
References (92)
- et al.
Environmental correlates of large-scale spatial variation in the delta C-13 of marine animals
Estuar. Coast Shelf Sci.
(2009) - et al.
Overexploiting marine ecosystem engineers: potential consequences for biodiversity
Trends Ecol. Evol.
(2002) - et al.
Correlations of amino acids in proteins
Peptides
(2003) - et al.
Gag Grouper, marine reserves, and density-dependent sex change in the Gulf of Mexico
Fish. Res.
(2012) - et al.
Examining mummichog growth and movement: are some individuals making intra-season migrations to optimize growth?
J. Exp. Mar. Biol. Ecol.
(2009) - et al.
Population structure of red snapper (Lutjanus campechanus) in US waters of the western Atlantic Ocean and the northeastern Gulf of Mexico
Fish. Res.
(2015) - et al.
Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans
Deep-Sea Res. Part II Top. Stud. Oceanogr.
(2015) - et al.
Seasonal delta C-13 and delta N-15 isoscapes of fish populations along a continental shelf trophic gradient
Continent. Shelf Res.
(2013) - et al.
Multiple regression models of δ13C and δ15N for fish populations in the eastern Gulf of Mexico
Continent. Shelf Res.
(2014) - et al.
Modeling the spatial distribution of commercially important reef fishes on the West Florida Shelf
Fish. Res.
(2013)
Teleost lens development and degeneration
International Review of Cell and Molecular Biology
Subtropical epibenthos varies with location, reef type, and grazing intensity
J. Exp. Mar. Biol. Ecol.
Gag grouper larvae pathways on the West Florida Shelf
Continent. Shelf Res.
Assessing residency and movement dynamics of swordfish Xiphias gladius in the Eastern North Pacific Ocean using stable isotope analysis
Mar. Ecol. Prog. Ser.
Investigations of selected parameters for growth of larval and juvenile black sea bass Centropristis striata L
J. World Aquacult. Soc.
Site fidelity and condition metrics suggest sequential habitat use by juvenile common snook
Mar. Ecol. Prog. Ser.
Seabasses (pisces: serranidae)
Mem. Hourglass Cruises
Disparity between planktonic fish egg and larval communities as indicated by DNA barcoding
Mar. Ecol. Prog. Ser.
Survival of Red Grouper (Epinephalus morio) and red snapper (Lutjanus campechanus) caught on J-hooks and circle hooks in the Florida recreational and recreational-for-hire fisheries
Bull. Mar. Sci.
DNA barcoding reveals clear delineation between spawning sites for neritic versus oceanic fishes in the Gulf of Mexico
Fish. Oceanogr.
Growth and relative size of calcified structures of fish
Trans. Am. Fish. Soc.
Reproductive styles of shallow-water groupers (Pisces: serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations
Environ. Biol. Fish.
Benthic habitat modification through excavation by red grouper, Epinephelus morio, in the northeastern Gulf of Mexico
Open Fish Sci. J.
Groupers on the edge: shelf edge spawning habitat in and around marine reserves of the northeastern Gulf of Mexico
Prof. Geogr.
Aggregation spawning: biological aspects of the early life history
Development from egg to juvenile of the red grouper (Epinephelus morio) (pisces: serranidae) in the laboratory
Rapid, accurate, and non-invasive measurement of Zebrafish axial length and other eye dimensions using SD-OCT allows longitudinal analysis of myopia and emmetropization
PloS One
Stable isotope analysis of eye lenses from invasive lionfish yields record of resource use
Mar. Ecol. Prog. Ser.
Hunting high or low: body size drives trophic position among and within marine predators
Mar. Ecol. Prog. Ser.
Relating otolith chemistry to surface water chemistry in a coastal plain estuary
Can. J. Fish. Aquat. Sci.
Larval development of red snapper, Lutjanus campechanus, and comparisons with co-occurring snapper species
Fish. Bull.
Spatial and temporal patterns in fertilization and settlement of young gag (Mycteroperca microlepis) along the west Florida shelf
Bull. Mar. Sci.
Diatom sources of C-13 rich carbon in marine food webs
Mar. Ecol. Prog. Ser.
A rapid ontogenetic shift in the diet of juvenile Yellowfin Tuna from Hawaii
Mar. Biol.
Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems
Evaluation of Trace-Metal and Isotopic Records as Techniques for Tracking Lifetime Movement Patterns in Fishes, College of Marine Science
Temporal persistence of Red Grouper holes and analysis of associated fish assemblages from towed camera data in the Steamboat Lumps marine protected area
Trans. Am. Fish. Soc.
Seasonal diet shifts and trophic position of an invasive cyprinid, the Rudd Scardinius erythrophthalmus (Linnaeus, 1758), in the upper Niagara River
Aquat. Invasions
Reconstructing marine life-history strategies of wild Atlantic salmon from the stable isotope composition of otoliths
Mar. Ecol. Prog. Ser.
The Florida Gulf of Mexico continental shelf—great contrasts and significant transitions
Age, growth, reproduction, and the feeding ecology of black-sea bass, Centropristis striata (Pisces, Serranidae), in the eastern Gulf of Mexico
Bull. Mar. Sci.
Emerging from Hjort's shadow
J. Northwest Atl. Fish. Sci.
Comparison of Isotope-Based Biomass Pathways with Groundfish Community Structure in the Eastern Gulf of Mexico, College of Marine Science
Comparing isotopic niche widths among and within communities: SIBER - stable Isotope Bayesian Ellipses in R
J. Anim. Ecol.
Age-size structure of red grouper, (Epinephelus morio), from the eastern Gulf of Mexico
Northeast Gulf Sci.
Between-reader bias and variability in the age-determination process
Fish. Bull.
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