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, 94 (6), 1947-1973

Beyond Trophic Morphology: Stable Isotopes Reveal Ubiquitous Versatility in Marine Turtle Trophic Ecology

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Beyond Trophic Morphology: Stable Isotopes Reveal Ubiquitous Versatility in Marine Turtle Trophic Ecology

Christine Figgener et al. Biol Rev Camb Philos Soc.

Abstract

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta-analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub-specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource-axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non-exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over-predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.

Keywords: animal personality; cryptic dietary diversity; ecoinformatics; ecological exchangeability; ecological partitioning; interspecific competition; intraspecific competition; marine food webs; niche variation hypothesis; trophic variability.

Figures

Figure 1
Figure 1
Nested, hierarchical contextualization of trophic variation and studies exemplifying concept in conceptual (Co), theoretical (T), and empirical (E) ways. Trophic variation occurs: (A) among species in adaptive/ecological radiations; (B) among populations, within species; (C) within populations [among different life stages (C.1) and between sexes (C.2)], and (D) among individuals. CLC, complex life cycles.
Figure 2
Figure 2
Schematic illustration summarising current knowledge about sea turtle life cycles and their associated marine macrohabitats (modified from Bolten, 2003). (A) Depiction of the three distinct macrohabitats (terrestrial, neritic, oceanic) inhabited by different marine turtle life stages. (B) The three types of life‐history patterns among marine turtle species depicting the sequential use of the three macrohabitats by different developmental stages. In all three panels, solid boxes depict well‐documented associations between life stages and macrohabitats, and solid arrows depict known movements of life stages between macrohabitats. Dashed boxes and arrows depict hypothesised but undocumented associations and movements. The red box and dashed arrows reflect a novel finding of an additional life stage–macrohabitat association of juvenile C. caretta ($) and adult C. caretta and C. mydas (*) based on stable isotope analyses (Eder et al., 2012; Hatase et al., 2010, 2013, 2006; McClellan et al., 2010; McClellan & Read, 2007). The Type 1 life cycle is exhibited by N. depressus. The Type 2 life cycle is exhibited by C. caretta, C. mydas, E. imbricata and L. kempii. The Type 3 life cycle is exhibited by D. coriacea and L. olivacea.
Figure 3
Figure 3
Comparative overview of the trophic morphology of extant marine turtle species. The left panels (i) depict lateral views of the skulls; the darker colouration depicts the keratinous sheaths (also called beak or rhamphotheca) that covers the jaws in the six species of Cheloniidae. The single species of Dermochelyidae, D. coriacea, lacks a rhamphotheca but possesses skin covering the jaws, which is shown in darker colouration. The middle panels (ii) depict dorsal views of the inside of the lower jaw and the right panels (iii) depict ventral views of the inside of the upper jaw. These artist's renderings are based on museum specimens housed in the Chelonian Research Institute. High‐resolution versions of these illustrations are provided in Fig. S1. Illustrations by Dawn Witherington.
Figure 4
Figure 4
Summary of predicted and observed spatial foraging strategies (δ13C, A, B) and trophic position (δ15N, C, D) of adults of six marine turtle species (Cc, C. caretta; Cm, C. mydas; Dc, D. coriacea; Ei, E. imbricata; Lk, L. kempii; Lo, L. olivacea). A and C show our predictions (see Section IV.1), and B and D show the species' least‐square means (LSMs) from the linear mixed‐effect models (see Table 3). Statistically significant differences among species determined using Tukey honest significant difference (THSD) post hoc tests are indicated by different letters; species that share a letter are not significantly different. In A and B the life‐cycle macrohabitat type (see Fig. 2) is indicated for each species.
Figure 5
Figure 5
Scatterplot of 91 means from estimates of δ13C and δ15N in adults of six marine turtle species (C. caretta, dark grey circle; C. mydas, green cross; D. coriacea, blue triangle; E. imbricata, orange inverted triangle; L. kempii, red diamond, L. olivacea, red square) within four ocean basins (Atlantic ocean, filled symbols; Mediterranean sea, large plus signs within symbols; Indian ocean, small plus signs within symbols; Pacific ocean, open symbols) Each point represents a single population. Data are summarised in Figgener et al. (2019) and raw data can be found in Dryad (https://doi.org/10.5061/dryad.3v060tq). A maximum convex hull is drawn around all points for a given species to facilitate visual comparison.

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