Stable Isotopes in Fish Eye Lenses as Potential Recorders of Trophic and Geographic History

Abstract

We evaluated eye lenses as potential recorders of stable isotope histories in fish because they consist of metabolically inert optical proteins that are deposited in successive, concentric circles (laminae) much like otolith circuli and tree rings. We conducted four different tests on lenses from red snapper, red grouper, gag, and white grunt. The first test was a low-resolution screening of multiple individuals (4–5 radial groups of laminae per lens, all species except white grunt). Along the radial axis, all individuals exhibited substantial isotopic variability. Red snapper individuals separated into two groups based on δ 15N and gag separated into two groups based on δ 13C. Two gag with the greatest variation were chosen for high-resolution temporal analysis using individual laminae from their second eye lenses. The first-order patterns from the high-resolution analysis generally mimicked patterns from the low-resolution screening of grouped laminae, yet the high-resolution plots revealed early-life details that were not apparent in the low-resolution screenings. For the third test, left- versus right-eye variation was compared using high-resolution methods. White grunt left- and right-eye radial isotopic patterns were almost identical for both δ 13C and δ 15N, suggesting the variations observed among individual fish were not artifacts. The final test evaluated intra-laminar variation; multiple samples were analyzed from different parts of the same lamina. Seven laminae from three individuals of two species were analyzed in this manner; variations among laminae were found to be much higher than variations within laminae. However, nominal intra-laminar variations were comparable to nominal differences between left and right lenses, suggesting intra-laminar variation established measurement precision. Eye lens isotopes appear to be useful for reconstructing the isotopic histories of individual fish; these histories can be compared with spatially-derived isoscapes to reconstruct individual histories for site fidelity, movement and trophic position.

Chemical archives in fishes beyond otoliths: A review on the use of other body parts as chronological recorders of microchemical constituents for expanding interpretations of environmental, ecological, and life‐history changes

“…While some findings suggest that scale Sr : Ca correlates with concentrations in ambient water and otoliths (Wells et al 2003a;Campbell et al 2015), others have found no such relationship (Clarke et al 2007). Complicating the matter, Weakfish (Cynoscion regalis) scale and otolith Sr : Ca were found to be dissimilar in 1-yr-old fish but comparable at age two, possibly due to elemental remobilization in older individuals (Wells et al 2003b). Courtemanche et al (2006) noted that even the subset of scales chosen for analysis affected the detection of a Sr : Ca correlation between otoliths and scales, and suggested scales may become an unreliable indicator of Sr once diadromous fish encounter the marine environment.…”

“…Other exploratory work has been conducted on squid lenses; squid have a complex eye much like vertebrates (Parry 2003;Hunsicker et al 2010). Wallace et al (2014) also called for further experimentation with respect to aging eye lenses as well as conducting compound specific isotope analyses.…”

“…Even among nonvascular alternatives, elemental values may not correlate with those of otoliths due to physiological pathway differences (Gillanders 2001). In cases of poor or unknown elemental agreement with other structures, it is still possible that comparisons of a single alternative structure can be made among individuals without correlating its patterns with those of other structures (Arai et al 2002;Allen et al 2009;Wallace et al 2014).…”

Skating on thin ice: Identifying the need for species‐specific data and defined migration ecology of Rajidae spp.

“…Another alternative, albeit relatively unexplored, tissue type which can be used to estimate longevity, and reconstruct lifetime patterns of movement and migration of fishes is the eye lens (Nielsen et al., ; Quaeck‐Davies et al., ; Wallace, Hollander, & Peebles, ). The eye lens is useful for species which do not possess hard structures such as otoliths (e.g., elasmobranchs), or in cases where vertebral sampling cannot be conducted (e.g., endangered species or tagged fish).…”

“…The eye lens is useful for species which do not possess hard structures such as otoliths (e.g., elasmobranchs), or in cases where vertebral sampling cannot be conducted (e.g., endangered species or tagged fish). Fish eye lenses are metabolically inert and incrementally grown in concentric layers called laminae (Dahm, Schonthaler, Soehn, Van Marle, & Vrensen, ; Wallace et al., ). The oldest cells reside within the central core, whereas the newest layers are deposited at the lens margin (Quaeck‐Davies et al., ; Wallace et al., ).…”