Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

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.

Full text

Biol. Rev. (2019), pp. 000–000. 1
doi: 10.1111/brv.12543
Beyond trophic morphology: stable isotopes
reveal ubiquitous versatility in marine turtle
trophic ecology
Christine Figgener1,2,3∗, Joseph Bernardo1,2,4 and Pamela T. Plotkin1,3,5
1Marine Biology Interdisciplinary Program, Texas A&M University, 3258 TAMU, College Station, TX 77843, U.S.A.
2Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, U.S.A.
3Department of Oceanography, Texas A&M University, 3146 TAMU, College Station, TX 77843, U.S.A.
4Program in Ecology and Evolutionary Biology, Texas A&M University, 2475 TAMU, College Station, TX 77843, U.S.A.
5Texas Sea Grant, Texas A&M University, 4115 TAMU, College Station, TX 77843, U.S.A.
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
* Author for correspondence (Tel.: (1) 979-985-0831; E-mail: christine.figgener@tamu.edu).
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original
work is properly cited.

2Christine Figgener and others
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.
Key words: niche variation hypothesis, ecological partitioning, trophic variability, cryptic dietary diversity, marine food
webs, ecoinformatics, interspecific competition, intraspecific competition, animal personality, ecological exchangeability.
CONTENTS
I. Introduction .............................................................................................. 2
II. Background .............................................................................................. 4
(1) Marine turtles as a model system of ecological partitioning ........................................... 4
(2) Marine turtle life cycles ............................................................................... 9
III. Methods .................................................................................................. 9
(1) Literature review ..................................................................................... 9
(2) Meta-analysis ......................................................................................... 10
IV. Results ................................................................................................... 12
(1) Variation in trophic ecology among species – a meta-analysis ....................................... 12
(2) Variation in trophic ecology among populations ..................................................... 13
(3) Variation in trophic ecology within populations ...................................................... 15
(a) Variation in trophic ecology among life stages .................................................... 15
(b) Variation in trophic ecology between sexes ....................................................... 17
(4) Variation in trophic ecology among adults within a population and its effect on individual fitness ... 17
V. Discussion ................................................................................................ 18
(1) Novel insights about marine turtle trophic ecology from stable isotope analysis ...................... 19
(2) Implications for marine turtle conservation and management ........................................ 19
(3) Ecological roles of marine turtles in the marine realm ................................................ 20
(4) Implications for future research on ecological radiations ............................................. 21
VI. Conclusions .............................................................................................. 21
VII. Acknowledgments ........................................................................................ 21
VIII. References ................................................................................................ 21
IX. Supporting Information .................................................................................. 27
I. INTRODUCTION
A key premise of Darwinian evolution is that, because
resources are limited, competition is a fundamental driver of
evolutionary change. Darwin (1859) argued that interspecific
competition causes a ‘struggle for existence’, which ‘will
generally be most severe between those forms which are
most nearly related to each other in habits, constitution, and
structure’ (p. 112). Using this logic, he further hypothesised
that resource competition should be more intense within
a species than among species. Intraspecific competition
occurs among life stages (e.g. between juveniles and adults),
between the sexes, and even among individuals within the
same life stage and sex. Thus, competition is a continuum
encompassing multiple hierarchical levels from interspecific
to different levels within species (Fig. 1). Since Darwin’s
(1859) seminal arguments, ecologists and evolutionary
biologists have produced an enormous body of theoretical,
conceptual and empirical work that explores how organisms
ameliorate both inter- and intraspecific competition across
all of these hierarchical levels (Fig. 1).
As Darwin (1859) noted, competition is likely most
severe among species that are similar in morphology and
other attributes, so competition has been studied intensely
in adaptive radiations. Adaptive radiation is the process
in which organisms diversify rapidly from an ancestral
line into a variety of new forms occupying different
adaptive zones (Simpson, 1944; Schluter, 2000). A review
of vertebrate examples found that radiations unfold through
stereotyped stages of diversification, beginning with habitat
differentiation and followed by the evolution of divergent,
irreversible morphological structures related to divergent
trophic ecology (Streelman & Danley, 2003). Because studies
of radiations have largely been retrospective, they have
typically focused on the terminal and most obvious stage
of divergence, morphological divergence, as a proxy to
quantify trophic variation among species. Nonetheless, it
has been possible to infer the earlier stages by correlating
early speciation events with contemporary differences in
habitat use.
By contrast, other studies have tried to assess the
competitive dynamics of early stages of radiations by
examining initial divergence in habitat and morphology
and how they relate to trophic ecology using intraspecific
systems. Many of the best-studied examples are from fish that
have colonised post-glacial lakes, which show a consistent
signal of foraging habitat segregation (e.g. benthic versus
pelagic ecomorphs in fish that have colonised post-glacial
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Beyond Trophic Morphology 3
Fig. 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.
lakes (Schluter, 2000) accompanied by morphological
manifestations of trophic divergence (Berg et al., 2010;
Harrod, Mallela & Kahilainen, 2010; Kahilainen et al.,
2004; Knudsen et al., 2006; Muir et al., 2016; Præbel
et al., 2013; Schluter, 1993, 1995; Schluter & McPhail,
1992). Even in these examples that examine the putative
early stages of radiation, it is extremely difficult to
detect a foraging habitat difference without having some
signal of morphological differentiation. Notable exceptions
come from experimental studies of host-race formation in
insects, in which host-specialisation evolves without obvious
morphological divergence (Feder, Chilcote & Bush, 1988;
Feder et al., 2003; Smith & Sk´ulason, 1996; Via, 1999).
It stands to reason that if foraging habitat diversification is
indeed the first stage of radiation, it must be more prevalent
than currently recognised because a lack of morphological
variation does not necessarily indicate a lack of divergence in
habitat use. Most research still mainly relies on morphological
differences to recognise that there was an earlier divergence
in habitat use. Another reason why divergence in habitat
use may also be more common than currently recognised
is that detecting divergence in habitat use requires as a first
step direct observation of organisms and their pattern of
habitat use. This is challenging in species that are difficult to
observe, such as those that occupy remote habitats, occur at
very low densities, or are highly migratory. We define this
undetected habitat divergence that is unaccompanied by a
morphological signal as cryptic habitat specialisation.
Although Darwin (1859) recognised that intraspecific
competition is likely more severe than interspecific
competition, analyses of the mechanisms by which
species ameliorate it has lagged far behind analyses of
interspecific competition. Ecological niches have typically
been characterised at the species level, which implicitly
assumes a typological ecology for a given species.
However, the niche of a species is the joint response
of subpopulations, groups, and individuals to complex
ecological and evolutionary processes (Semmens et al., 2009).
Thus, the collective differences in niches across relevant
levels of hierarchies comprise the niche of a species, known
as niche variability (Van Valen, 1965; Semmens et al.,
2009). Despite early theoretical (Van Valen, 1965) and
empirical (Schoener, 1967, 1968) work aimed at elucidating
competitive intraspecific dynamics, detailed consideration
of this problem has only emerged in the last three decades.
These include analyses of how ontogenetic variation (Werner
& Gilliam, 1984), sex-specific differences (Butler, Schoener &
Losos, 2000; Schoener, 1967), and inter-individual variation
(Araujo, Bolnick & Layman, 2011; Bolnick et al., 2007b;
Violle et al., 2012) relate to competition (Fig. 1).
The first clear treatment of intraspecific competition was
advanced by Van Valen (1965). This idea, now known as the
niche-variation hypothesis (NVH), predicts that populations
with wider niches (generalists) are more variable than
populations with narrow niches (specialists). As has been
the case in analyses of interspecific competition, a search
for morphological differences, usually in size, has been
the dominant approach in attempts to discover whether
individuals within a species partition resources (Schoener,
1967, 1968, 1984; Werner & Gilliam, 1984; Werner & Hall,
1988; Butler, Schoener, & Losos, 2000) according to the
NVH. Many studies that have taken this approach have
failed to detect evidence of intraspecific resource partitioning
(Bolnick et al., 2007b). But again, a morphology-driven
approach is likely to underestimate the extent of ecological
partitioning among individuals, because such variation
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

4Christine Figgener and others
can arise due to behavioural decisions concerning habitat
use or prey choice and is not necessarily mediated by
morphological phenotypes (Bolnick et al., 2007b). This insight
has developed from studies that directly examine dietary
variation [gut content analysis (Bolnick et al., 2007b;Costa
et al., 2008)]. Both of the latter studies found that more
generalised populations exhibit higher among-individual
variation, supporting general predictions of the NVH.
A powerful tool to evaluate the NVH beyond trophic
morphology is stable isotope analysis (SIA). Although it has
not yet been widely applied to test the NVH per se,SIA
has provided novel insights on diversification in trophic
ecology and habitat use. This approach has confirmed that
morphological variation alone may underestimate true levels
of trophic diversification. For instance, SIA of aquatic insects,
in which there is a strong tradition of assigning species to
trophic levels (functional groups) based on their mouthparts,
reveals polyphagy across trophic levels not predicted by
their trophic morphology (F¨ureder, Welter & Jackson, 2003;
Lancaster et al., 2005; Mihuc & Toetz, 1994; Miyasaka &
Genkai-Kato, 2009).
Stable isotopes are intrinsic markers that are assimilated
through the food, water, and gas that enter the body
(Rubenstein & Hobson, 2004). The two most commonly
used stable isotopes for studies of trophic ecology are stable
carbon (13C) and stable nitrogen (15 N). A consumer’s stable
isotope composition or value is determined by the ratio of
light to heavy isotopes (e.g. 12C:13 Corδ13C) of its dietary
sources (Hobson, 1999). Due to the selectivity of heavier
isotopes during metabolic processes, animal tissues tend
to be enriched relative to their diet by a discrimination
factor of 0–1‰ for δ13C (DeNiro & Epstein, 1978) and
3–4‰ for δ15N per trophic level (DeNiro & Epstein, 1981),
depending on the tissue surveyed. SIA utilises this predictable
discrimination from source to consumer to make ecological
predictions. In the marine environment, δ13C values reflect
the value of primary producers in a food chain, which in turn
indicates the type of habitat in which an organism is foraging
(DeNiro & Epstein, 1978; Hobson, 1999; Rubenstein &
Hobson, 2004). Stable nitrogen indicates the trophic position
of an organism within its food chain (DeNiro & Epstein,
1981; Hobson, 1999; Rubenstein & Hobson, 2004). Taken
together, the combination of δ13Candδ15N values provides a
quantitative isotopic niche, and thus characterises the overall
trophic ecology of an individual.
Over the past two decades, SIA has been widely applied
to study foraging history and strategies in a wide range of
species and biomes. SIAs have been an especially powerful
tool to characterise diets and illuminate trophic dynamics
in elusive species (e.g. marine or highly migratory). For
instance, in marine turtles – the subject of this review – SIA
has been used to reconstruct foraging histories of individuals
mainly observed in their breeding grounds (Ceriani et al.,
2012; Seminoff et al., 2012; Vander Zanden et al., 2015).
This body of work has revealed a greater level of complexity
in trophic ecology, both among and within species than
previously recognised.
In this systematic review, we examine the nature and
extent of interspecific and intraspecific variation across all
of the hierarchical levels of competition (Fig. 1) using a
novel synthesis of stable isotope data for six of the seven
extant marine turtle species. Because of conservation and
management concerns, a large number of marine turtle
populations and management units have been studied using
SIA to address a wide variety of questions including foraging
patterns and trophic level, habitat use, migration, population
connectivity, and physiology at a variety of spatial scales
(Figgener, Bernardo & Plotkin, 2019). Unfortunately, little
effort has been made to synthesise these findings to address
broader evolutionary and ecological questions.
Although these studies were conducted with diverse
aims, they provide an opportunity to examine larger-scale
signatures of hierarchical ecological partitioning among
marine turtles (Fig. 1). Our review has four main
components. We examined interspecific variation in trophic
ecology (A in Fig. 1) using a formal meta-analysis of adult
stable isotope values because there were sufficient data. We
also synthesised signals of intraspecific variation in trophic
ecology across three hierarchical levels (B–D in Fig. 1) using
a comparative, descriptive approach, because there were
insufficient data to permit a rigorous meta-analysis at these
levels. To our knowledge, no single study across all these
hierarchical levels has been conducted previously in any
ecological radiation.
II. BACKGROUND
(1) Marine turtles as a model system of ecological
partitioning
The crown group of marine turtles (Superfamily
Chelonioidea) evolved in the mid-Upper Cretaceous,
∼100–84 million years ago (MYBP) (Gentry, 2017; Pyenson,
Kelley & Parham, 2014). A rich fossil record indicates
that this radiation comprised up to 27 species that were
highly diversified morphologically and ecologically (Cadena
& Parham, 2015). The extensive fossil record of marine
turtles reveals a large continuum of differentiation along
several axes (Parham & Pyenson, 2010; Pyenson, Kelley, &
Parham, 2014; Cadena & Parham, 2015). The seven extant
species in this monophyletic group reflect this diversity.
The Family Cheloniidae is characterised by a keratinised
sheath (also called beak or rhamphotheca) covering their
jaw bones and a hard shell. It contains six species including
the green (Chelonia mydas Linnaeus, 1758), loggerhead (Caretta
caretta Linnaeus, 1758), Kemp’s ridley (Lepidochelys kempii
Garman, 1880), olive ridley (Lepidochelys olivacea Eschscholtz,
1829), hawksbill (Eretmochelys imbricata Linnaeus, 1766), and
flatback turtle (Natator depressus Garman, 1880). The Family
Dermochelyidae lacks a rhamphotheca and has a leathery
shell. It is monotypic, containing the leatherback (Dermochelys
coriacea Vandelli, 1761) (Table 1).
Marine turtles are an ideal model group to study ecological
partitioning among putative competitors for several reasons.
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Beyond Trophic Morphology 5
Table 1. Overview of the seven extant marine turtle species: common names, taxonomy, age at sexual maturity (ASM), nesting distribution, trophic ecology and body size.
1Spotila (2004); 2Bjorndal (1997); 3Bolten (2003); 4Eckert et al. (2012).
Average adult body size1
Common name Taxonomy ASM1
Nesting
distribution
(most northern
and southern)
Trophic
micro-habitat3/
diet2Carapace
length [cm] Mass [kg]
Life-history1: Clutch size
# Clutches per season
Remigration
interval
Loggerhead
turtle
Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Caretta
Caretta caretta (Linnaeus, 1758)
17–45 30◦N35
◦S benthic/hard-shelled
prey, crustaceans,
mollusks
85–124 80–200 97–127
3.9
2–4 years
Green turtle Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Chelonia
Chelonia mydas (Linnaeus, 1758)
26–44 30◦N23
◦S benthic/ seagrass,
algae
80–122 65–204 110
3
2.3–5 years
Hawksbill turtle Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Eretmochelys
Eretmochelys imbricata (Linnaeus, 1843)
17–25 27◦N24
◦S benthic/ sponges,
soft corals
75–88 43–75 130
3–5
2.9 years
Flatback turtle Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Natator
Natator depressus (Garman, 1880)
unknown 9◦S24
◦S benthic/ echinoderms,
shrimps, molluscs,
sea pens, bryozoans
75–99 70–90 54
2.8
2.6 years
Kemp’s ridley
turtle
Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Lepidochelys
Lepidochelys kempii (Garman, 1880)
11–21 35◦N18
◦N benthic/ crustaceans 61–76 36–45 110
3
1.5 years
Olive ridley
turtle
Superfamily: Chelonioidea
Family: Cheloniidae
Genus: Lepidochelys
Lepidochelys olivacea (Eschscholtz, 1829)
11–16 24◦N30
◦S Pelagic–benthic/
crustaceans, molluscs,
fish, algae
55–76 36–43 110
2–3
1.7 years
Leatherback
turtle
Superfamily: Chelonioidea
Family: Dermochelyidae
Genus: Dermochelys
Dermochelys coriacea (Vandelli, 1761)
12–29438◦N34
◦S pelagic/ soft-bodied
prey: jellyfish, sea
salps, tunicates
132–178 250–907 65–85
1–10
2–4 years
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

6Christine Figgener and others
The extant species differ from each other in several ways that
are typically associated with ecological radiations including
life-history traits (particularly body size), habitat use, and
trophic morphology. Further, the modern species have
exhibited morphological stasis over the last 30 million years,
suggesting that these differences represent stable ecological
strategies.
Thus, like other ecological radiations, the biology of
marine turtles simultaneously reflects both signs of resource
competition and ecopartitioning. Concerning life histories,
marine turtles are similar in some respects (e.g. clutch size,
egg size, breeding periodicity), but show striking variation in
others, especially body size (Hendrickson, 1980; Van Buskirk
& Crowder, 1994; Spotila, 2004). Body-size divergence
among related species is often implicated in the ecological
literature as a means of reducing competitive overlap (Smith
& Lyons, 2013). Marine turtles span one order of magnitude
in adult size from the leatherback turtle (D. coriacea), weighing
250–907 kg to the two ridley species (L. olivacea and L.
kempii), weighing 36 – 43 kg (Spotila, 2004). Within species,
the development from hatchling to adult passes through
more than two orders of magnitude (Spotila, 2004).
Similarly, concerning habitat use, marine turtles display
both spatial overlap and spatial partitioning. On the
one hand, marine turtles are highly migratory, travelling
thousands of kilometres from feeding grounds to breeding
grounds on tropical and subtropical beaches (Plotkin, 2003).
These extensive migrations imply broad spatial overlap of
ocean habitat. Five of the seven species are widely distributed
throughout several ocean basins (Table 1), but species differ
in their basin-wide and within-basin distributions (Spotila,
2004). The exceptions are N. depressus, which is endemic to
northern Australasian waters, and L. kempii, which mainly
inhabits the Gulf of Mexico, but uses other western Atlantic
waters. Additionally, most species are confined to tropical
and subtropical latitudes for nesting and foraging, except
C. caretta, which nests and feeds in temperate zones and
D. coriacea, which nests in the tropics and subtropics but
feeds in cold waters at high latitudes. All of these patterns
of broad-scale habitat use imply that marine turtles may
often compete for resources. Further, on a finer scale, up
to six species may be locally sympatric in regions within
ocean basins (see online Supporting information, Table S1).
At the finest scale, it is common for several species to overlap
in their breeding ranges and on nesting beaches with only
weak temporal separation. Often three but up to four species
may syntopically use breeding and foraging areas (Cornelius,
1986; Chacon et al., 1996; Chatto & Baker, 2008).
By contrast, it has long been appreciated that marine tur-
tles exhibit an ecological signature of radiation among habi-
tats (Hendrickson, 1980; Spotila, 2004), at both the ocean
basin (macrohabitat) and microhabitat scales (Table 1). At
the macrohabitat level, species partition the ocean spatially:
horizontally, with regard to the continental shelf (oceanic
versus neritic, Fig. 2) and vertically, with regard to bathymetry
(pelagic, demersal, and benthic, Table 1) (Bjorndal, 1997;
Bolten, 2003). Dermochelys coriacea and L. olivacea principally
forage pelagically in oceanic waters. All other species
principally forage in neritic waters using one or more layers
of the water column. At the microhabitat level, some species
are relatively specialised (e.g. seagrass beds, coral reefs)
(Table 1) and others are more generalised. These differences
in habitat use result in dietary differences, which are reflected
in analyses of gut contents (Table 1) (Bjorndal, 1997).
Finally, concerning trophic morphology, despite the fact
that all species have powerful, toothless jaws, the most
striking indication of ecopartitioning among marine turtles
is the remarkable divergence in the shape of their jaws
and beaks (Fig. 3, Fig. S1). The beak, or rhamphotheca,
comprises the rhinotheca covering the upper jaw and the
gnathotheca covering the lower jaw. The differences in
trophic morphology are recognised as feeding ecomorphs
based on trophic anatomy and gut-content analyses.
Correlations between trophic morphology and diet in marine
turtles have been proffered for both extant (Wyneken, 2003)
and fossil (Hirayama, 1994, 1997; Parham & Pyenson, 2010;
Gentry, 2017) marine turtles. Interspecific morphological
variation in other aspects of head and neck anatomy related
to feeding has also been described (Wyneken, 2001, 2003;
Jones et al., 2012), further substantiating a link between diet
and trophic anatomy.
One ecomorph that has been recognised in extant and
fossil species is related to durophagy, which is the reliance
upon hard-shelled prey, such as crustaceans and molluscs.
Two extant species are principally durophagous: C. caretta
has a robust rhamphotheca (Fig. 3Ai) and wide, crushing
surfaces inside the mouth (Fig. 3Aii,iii). Similarly, the
rhamphotheca of L. kempii is robust and bears wide ridges
for crushing (Fig. 3Dii,iii). Post-pelagic individuals feeding
in coastal waters have a preponderance of crabs and other
crustaceans in their diets, with some molluscs and fish.
They also consume algae and seagrasses (Burke, Morreale &
Standora, 1994; Burke, Standora & Morreale, 1993; Seney
& Musick, 2005; Shaver, 1991).
By contrast, D. coriacea (Fig. 3G) is a highly specialised
gelativore that feeds on gelatinous prey such as ctenophores,
salps (planktonic tunicates) and the planktonic medusae of
Cnidaria (Bleakney, 1965; Brongersma, 1969, 1970; Den
Hartog, 1979; Den Hartog & Van Nierop, 1984; Duron
& Duron, 1980; Duron, Quero & Duron, 1983; Eckert
et al., 2012; Paladino & Morreale, 2001), possibly owing
to the lack of a keratinized beak. This specialisation is
further reflected in its upper jaw (Fig. 3Gi), which bears
two tooth-like projections used to pierce the air bladders of
floating cnidarians (Paladino et al., 2001).
Another ecomorph, represented by E. imbricata (Fig. 3C),
is specialised for spongivory. Its jaws and rhamphotheca,
unlike those of all other species, are relatively elongated
and narrow (Fig. 3Cii,iii), terminating in a parrot-like beak
with sharp cutting edges (Fig. 3Ci). These morphological
attributes allow E. imbricata to scrape and cut sponges and
other reef-inhabiting anthozoans, such as soft corals and
anemones, from hard substrates (Witzell, 1983; Meylan,
1988; Anderes Alvarez & Uchida, 1994; Anderes Alvarez,
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Beyond Trophic Morphology 7
Fig. 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 (*)basedonstable
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.TheType3life
cycle is exhibited by D. coriacea and L. olivacea.
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8Christine Figgener and others
A
B
C
D
E
F
G
Fig. 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.
2000). It also detaches pieces of corals to access sponges in
the interstices of the reef.
The last ecomorph, represented by C. mydas, is specialised
for herbivory. Its gnathotheca (lower rhamphotheca;
Fig. 3Bii) bears serrated, sharply ridged edges that occlude
against the rhinotheca (upper rhamphotheca; Fig. 3Biii),
providing the capacity to shear blades of seagrasses, which
constitute the majority of their diet (Bjorndal, 1979, 1980,
1985; Forbes, 1993; Mortimer, 1981; Seminoff, Resendiz &
Nichols, 2002).
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Beyond Trophic Morphology 9
The remaining two species, L. olivacea and N. depressus,are
omnivorous, exhibiting both durophagous and gelativorous
feeding (Montenegro Silva, Bernal Gonzalez & Martinez
Guerrero, 1986; Zangerl, Hendrickson & Hendrickson,
1988) and their trophic morphology is so similar that
they were once thought to be closely related (Zangerl,
Hendrickson, & Hendrickson, 1988).
Lepidochelys olivacea is an opportunistic omnivore with a
widely varied diet. Studies of stranded turtles report a
high degree of durophagy and piscivory (Behera et al.,
2015; Colman et al., 2014; Di Beneditto, De Moura &
Siciliano, 2015; Spring & Gwyther, 1999; Wildermann &
Barrios-Garrido, 2012). Two studies of freshly killed turtles in
Mexico corroborated these findings, but also revealed a high
degree of gelativory (mostly salps, but also other tunicates)
as well as other soft-bodied prey including sipunculid
worms and bryozoans (Casas-Andreu & G´
omez-Aguirre,
1980; Montenegro Silva et al., 1986). Its trophic morphology
reflects this varied diet: L. olivacea has the most generalised
rhamphotheca in terms of shape and function (Fig. 3E).
Within this generalised morphology are several distinct
components related to feeding. First, the outer margins of the
rhamphotheca bear sharp, cutting edges (Fig. 3Ei). Second,
the gnathotheca bears a sharp, curved ridge along most of
its inner margin (Fig. 3Eii) which occludes with a similar
ridge on the rhinotheca. Third, the rhinotheca bears two
elongated, palatal cusps (Fig. 3Eiii), which are received by
two depressions in the gnathotheca (Fig. 3Eii) when the beak
closes. This functional complex acts like a mortar and pestle
to crush and grind hard-shelled prey. The last distinct feature
of the beak is that the rhamphotheca terminates in pointed
projections curving toward each other (Fig. 3Ei). This feature
functions similar to a pair of forceps, allowing for fine-scale
picking of small organisms from driftwood (C.F., personal
observations) or other substrates. The three-dimensional
relief of the rhamphotheca is not reflected by the underlying,
bony elements (Zangerl et al., 1988).
The other omnivore, N. depressus, consumes a wide
range of gelatinous and other soft-bodied prey including
siphonophores, bryozoans, holothurians, and jellyfish, as
well as hard-shelled prey such as molluscs (Zangerl et al.,
1988). This diet diversity is reflected in different components
of its trophic anatomy (Zangerl et al., 1988). It has a robust
rhamphotheca (Fig. 3F) bearing sharp cutting edges along the
outeredgeofthejaw(Fig.3Fi). Additionally, the rhinotheca
bears sharp-crested ridges along the posterior margin of the
secondary palate (Fig. 3Fiii). Between these cutting surfaces
is a flattened, triturating surface (Fig. 3Fiii). The gnathotheca
bears a very prominent, sharp-edged ridge along the inner
margin of the triturating surface, which comes to a sharp,
projecting point along the midline (Fig. 3Fii). However,
unlike in L. olivacea, these features are also reflected in the
underlying bony architecture of the mandible and the palate.
This summary of ecomorphological differentiation of
the seven species of marine turtles and concomitant
differentiation of their diets supports the hypothesis that
they ecopartition the oceanic realm (Hendrickson, 1980).
However, as is found in well-studied radiations, there also
remains some degree of dietary overlap.
(2) Marine turtle life cycles
An organism’s ecology is not defined only by its adult stage,
but rather its entire ontogeny (Wiens, 1982; Werner, 1988).
Marine turtle population models typically define distinct
life stages based on a size-class system: hatchling, juvenile,
subadult, and adult (Fig. 2) (Bolten, 2003; Crouse, Crowder
& Caswell, 1987; Heppell, Snover & Crowder, 2003), and
thus can be considered to have a complex life cycle, marked
by abrupt ontogenetic changes in behaviour and habitat
(Werner, 1988). All marine turtles, except N. depressus (Fig. 2B,
Type 1) (Bolten, 2003), share a general pattern of habitat
use among different life stages in which hatchlings migrate
from their natal beaches to oceanic nursery habitats (Fig. 2B,
Types 2 and 3), where they slowly swim or drift passively
within ocean currents (Wyneken & Salmon, 1992; Bjorndal,
1997; Boyle & Limpus, 2008; Mansfield et al., 2014). In the
case of C. caretta,C. mydas,E. imbricata,andL. kempii,after
attaining a threshold size, juveniles enter neritic development
habitats (Arthur, 2008; Bjorndal, 1997; Limpus, 1992; Reich,
Bjorndal & Bolten, 2007), where they spend most of their
lives even after attaining maturity (Fig. 2B, Type 2) (Bjorndal,
1997; Bolten, 2003). By contrast, D. coriacea and L. olivacea
adults range in the open ocean between nesting seasons
and little is known about juvenile and subadult stages after
the initial oceanic stages, but they are thought to remain
oceanic (Fig. 2B, Type 3) (Bjorndal, 1997; Plotkin, 2010;
Avens et al., 2013). After reaching maturity, adults of each
species migrate at intervals between foraging grounds and
distant nesting sites, with females exhibiting high site fidelity
over many years (Limpus, 1992; Balazs, 1994; Miller, 1997;
Plotkin, 2003). Males also exhibit site fidelity, returning to
the same breeding areas (waters adjacent to nesting beaches)
annually for mating (Hays et al., 2010; James, Eckert &
Myers, 2005a; Plotkin, 2003; Plotkin et al., 1996).
III. METHODS
(1) Literature review
We conducted a systematic review of 130 studies analysing
stable isotopes in marine turtle tissues and summarised those
(N=113) that are primarily concerned with the foraging
ecology of marine turtles using δ13Candδ15 N values. Our
aim was to analyse interspecific differences and highlight
examples of intraspecific and intrapopulation variation in
isotopic niche and its possible effects on the mitigation of
competition at different hierarchical levels (Fig. 1). Tables S2
and S3 summarise the distribution of studies among species,
basins, and broader study topics. A detailed description of
the selection and review process, as well as a summary of the
data set, is available in Figgener, Bernardo, & Plotkin (2019).
The full data set is available as MarTurtSI database on Dryad
(https://doi.org/10.5061/dryad.3v060tq).
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10 Christine Figgener and others
Table 2. Summary statistics of δ13Candδ15 N values from 91 data points for adult marine turtles used in our meta-analysis
δ13C values δ15N values
Range Range
Species NCV Minimum Maximum CV Minimum Maximum
Cheloniidae Caretta caretta 48 −0.0932 −18.9 −11.4 0.209 7.3 16.6
Chelonia mydas 9−0.300 −17.4 −7.6 0.204 5.1 9.2
Eretmochelys imbricata 4−0.092 −17.9 −14.4 0.226 5.9 10.5
Lepidochelys kempii 1NA −17.9 −17.9 NA 11.2 11.2
Lepidochelys olivacea 7−0.074 −18.4 −15.5 0.157 9.7 14.3
Dermochelyidae Dermochelys coriacea 22 −0.058 −21.1 −16.4 0.135 9.5 16.2
CV, coefficient of variation.
(2) Meta-analysis
In addition to the literature review, we used this novel
data synthesis to conduct a meta-analysis of stable isotope
composition of adults across six species to seek emergent
patterns by comparing among-species differences, and place
them into the general context of marine turtle ecology and
evolution. We assessed whether interspecific variation in
trophic niche suggested by previous studies is reflected in
isotopic values. We confined our analysis to adults for two
reasons. First, there is substantial and complex ontogenetic
variation in isotopic values among immature life-history
stages (see Section IV.3a). Second, growth rate has been
shown to affect the fractionation and resulting tissue isotope
values (Reich, Bjorndal & del Rio, 2008; Vander Zanden
et al., 2012), but because growth slows significantly after
turtles attain sexual maturity, comparisons among adults are
more straightforward (Chaloupka & Limpus, 1997; Limpus
& Chaloupka, 1997).
We obtained mean values of δ13Candδ15 N estimated
in adult individuals from published studies of six species
(there are no studies of N. depressus) (Table 2). We accepted
means from studies of any tissue that reported the origin
of samples, sample size, and either standard deviation or
standard error within one nesting population or foraging
area. Alternatively, we also accepted values from studies
for which we could compute means and standard errors
from either full supplementary data sets if available, or
from published graphs from which we extracted raw data
using PlotDigitizer 2.6.8 (Huwaldt, 2001). In cases where
multiple estimates existed for the same species or populations
from different studies, workers, or localities, we accepted
all estimates. The full data set used in this meta-analysis
is available in Dryad as part of the MarTurtSI database
(Figgener et al., 2019).
Fifty studies yielded 91 mean stable isotope values that
met the minimum selection criteria for inclusion in the
meta-analysis (Figgener et al., 2019) (doi: 10.5061/dryad
.3v060tq). The resulting data set was unbalanced in several
ways. First, there is a great deal of variation in the number
of observations for each species, with C. caretta yielding
most data points (N=48), only one study of L. kempii,
and none for N. depressus (Table 2). Second, not all ocean
basins were surveyed with the same effort (more studies
in the Atlantic than any other ocean basin). Additionally,
when comparing different ocean basins, stable isotope
composition might vary independently of actual differences
in foraging strategies, because basins differ in their nutrient
cycles and oceanographic features (McMahon, Hamady &
Thorrold, 2013). Third, there was great heterogeneity in
which tissues were sampled across species, with skin being
the most common. For example, one species might have
been studied using one tissue in one basin and a different
tissue in another (see also Pearson et al., 2017). Comparing
stable isotope values estimated from different tissues could
be problematic because they have different discrimination
factors depending on inherent synthetic pathways (Biasatti,
2004; Reich, Bjorndal, & del Rio, 2008; Seminoff et al.,
2009, 2006), and also reflect different times in the foraging
history of an individual (Rosenblatt & Heithaus, 2012).
Further, we lack a comprehensive framework to compare
stable isotope values across all combinations of sampled
tissues and across all species. Although a few studies have
proposed conversion factors for some pairs of tissues, they
were typically within a single species and life stage (Ceriani
et al., 2014; Kaufman et al., 2014; Tomaszewicz et al., 2017a).
Hence, there is no common currency that would permit
standardised comparison across all tissues. As a result, the
imbalance of the data and the noise introduced by comparing
different ocean basins and different tissues dictated the type
of analyses we were able to conduct.
We used current understanding of marine turtle foraging
ecology and stable isotope gradients in the marine realm
(Rubenstein & Hobson, 2004) to generate two a priori
predictions (Fig. 4A, C) of the rank order among species
for δ13Candδ15N values. The first prediction (Fig. 4A)
concerns expected spatial foraging strategies (reflected by
δ13C) as suggested by studies of spatial macrohabitat use
(Fig. 2) (Bolten, 2003; Plotkin, 2003) and microhabitat use
(Table 1) (Bjorndal, 1997). The second prediction (Fig. 4C)
concerns the expected trophic level of each species (reflected
by δ15N) based on general diets as suggested by studies of gut
contents and known prey species (Table 1) (Bjorndal, 1997),
as well as a previous study that determined the trophic level of
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Beyond Trophic Morphology 11
Fig. 4. Summary of predicted and observed spatial foraging strategies (δ13 C, 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.
juvenile and adult C. caretta,C. mydas,andD. coriacea in three
sampling locations using stable isotopes (Godley et al., 1998)
To gain an overview of species differences as well as
intraspecific variation in the data, we first plotted all δ13C
values versus δ15N values (Fig. 5). Further, to understand
inter- and intraspecific variation due to tissue and basin,
we conducted exploratory data analyses by first comparing
species-specific isotope values obtained from different tissues
but within a single basin (Atlantic, the basin with most
estimates) and second comparing species-specific isotope
values obtained from different basins but within the same
tissue (skin, the tissue with most estimates). In these analyses
we computed separate nested analyses of variance (ANOVAs)
of the ratios of each isotope (13C, 15 N) within a single basin
and tissue, respectively (Table S4, Table S5, Fig. S2). We
took among-tissue and among-basin effects into account in
our subsequent hypothesis-testing model.
We evaluated our a priori hypotheses concerning
interspecific differences in stable isotope composition
reflecting spatial foraging strategy (δ13C) and trophic level
(δ15N), and their rank order among species in three steps.
First, to evaluate whether there are interspecific
differences, we fitted two separate linear mixed-effect models
for each isotope using the lme4 package (Bates et al., 2015) in
R (R Core Team, 2018). The first model contained species as
a fixed factor and tissue (1—Tissue), basin (1—Basin), and an
interaction term between tissue and basin (1—Tissue:Basin)
as random, blocking factors to account for the heterogeneity
and unbalance of the data described above. The second
model only included the random, blocking factors. To test
for the overall effect of species, we then compared the two
models using the Akaike Information Criterion (AIC) and
performed a conditional F-test using the Kenward–Roger
approximation (Luke, 2017) with the pbkrtest package in
R (Halekoh & Højsgaard, 2014) To test for pairwise
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12 Christine Figgener and others
Fig. 5. Scatterplot of 91 means from estimates of δ13 Candδ15 N 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.
species’ differences, we computed Tukey Honestly Significant
Difference tests (THSDs) of the resulting least-squares means
between species using the multcomp package (Hothorn, Bretz
& Westfall, 2008).
Second, to compare the rank order of species against our
a priori predictions we used Spearman rank correlation on
all estimates and separately on the least-squares means from
the linear mixed-effect models. The Spearman correlation
coefficient (ρ)ranges from +1 (perfect association) to −1
(inverse association); a ρof zero indicates no association
between ranks.
Lastly, to evaluate intraspecific differences we calculated
the coefficient of variation for each species (Table 2,
Table S6).
IV. RESULTS
(1) Variation in trophic ecology among species – a
meta-analysis
Our meta-analyses of stable isotope composition across
six species and multiple ocean basins is the first
comprehensive synthesis that permits objective evaluation
of the long-standing hypothesis that marine turtle species
effectively ecopartition the marine realm (A in Fig. 1).
Our comparison of the paired mixed-effect models
(conducted for δ13Candδ15N separately) testing for species
differences indicated that the models including species
performed far better than the models that did not include
species (Table 3): the effect of species was highly significant
for both 13C(F(5) =25.438, P(>F)=6.451e−15)and15N
(F(5) =9.7253, P(>F)=3.628e−07) (Table 3). The total
random variation not explained by species is 2.8% for
δ13C, and 5.4% for δ15 N. Of the random variation in
δ13C not explained by species only about 2% was due to the
interaction of tissue and basin, 28% was due to tissue, 10%
was due to basin, and the remaining 60% was unexplained
by either factor. Of the random variation in δ15Nnot
explained by species only 11% was due to the interaction
of tissue and basin, 37% was due to tissue, 18% was due
to basin, and the remaining 34% was unexplained by either
factor.
The THSD post hoc tests revealed three distinct spatial
foraging strategies (δ13C) and two distinct clusters of trophic
levels (δ15N) among the six species for which data were
available. With respect to spatial foraging strategy (Fig. 4B),
C. mydas (group a) was distinct from all other species; E.
imbricata and C. caretta comprised a second group (group b)
and D. coriacea a third (group c). Both species of Lepidochelys
were intermediate and not significantly different from groups
b or c. The Spearman rank-order correlation between
our a priori species ranks of δ13 C values (Fig. 4A) and
both all estimates and the least-squares mean species ranks
was significant (ρALL(4) =0.81, P=0.05; ρLSQM (4) =0.81,
P=0.05). With respect to δ15N values (Fig. 4D), while two
significantly different groups were identified (a and d), the
differences were not as distinct for δ15Nastheywerefor
δ13C, owing to larger intraspecific variance than in δ13 C
values. Nonetheless, the Spearman correlation of our a
priori predictions of δ15N was significant (ρALL (4) =0.89;
P=0.025; ρLSQM(4) =0.83; P=0.025).
The congruence between the rank orders of our a priori
predictions based on spatial foraging strategy, gut content
analyses, and trophic morphology, and the rank order of the
stable isotope estimates broadly corroborates the hypothesis
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Beyond Trophic Morphology 13
Table 3. Summary of two linear mixed-effect models that were used to test for the effect of species in explaining the variation in
values among marine turtle species within each of two isotopes (13Cand15N). Species was treated as fixed factor, and tissue and
basin as random blocking factors. In addition, a random term for the interaction between tissue and basin was included
# Model AIC Marginal R2Conditional R2
δ13C1δ13 C∼Species +(1|Tissue) +(1|Basin) (1|Tissue:Basin) 327.131 0.553 0.729
2δ13C∼(1|Tissue) +(1|Basin) (1|Tissue:Basin) 410.378 NA NA
δ15N1δ15 N∼Species +(1|Tissue) +(1|Basin) (1|Tissue:Basin) 346.045 0.285 0.756
2δ15N∼(1|Tissue) +(1|Basin) (1|Tissue:Basin) 397.200 NA NA
AIC, Akaike Information Criterion.
of ecopartitioning among marine turtle species (Fig. 4).
However, far more complexity and overlap among species
are revealed by the stable isotope data (Fig. 5, Fig. S2).
Spatial patterns in foraging for adults as predicted
by the patterns in Fig. 2 are expected to correlate with
δ13C values because oceanic primary producers (planktonic
macroalgae and marine phytoplankton) primarily use the
C3photosynthetic pathway (Fry, 1996), whereas terrestrial
plants, the source of most nearshore carbon, use both C3
and C4/crassulacean acid metabolism (CAM) photosynthetic
pathways. This results in very distinct signatures for oceanic
and near-shore habitats (Rubenstein & Hobson, 2004).
Additionally, the δ13C values of seagrasses (e.g. genera Zosta
and Halophila), a principal component of the diet of C. mydas,
resemble those of terrestrial C4plants (Andrews & Abel,
1979; Beer, Shomer-Ilan & Waisel, 1980; Hemminga &
Mateo, 1996).
While the pattern we observed in δ13C was congruent with
our predictions based on assignment of species according
to macrohabitat (neritic versus oceanic) and microhabitat
(benthic, pelagic etc.) use, the three significantly distinct
groups (Fig. 4B) did not perfectly coincide with adult spatial
life-cycle patterns (Fig. 2). Group a comprised a single species,
the coastally foraging and largely herbivorous C. mydas which
was distinct from all other species including others sharing
the Type 2 life-cycle pattern (C. caretta,E. imbricata,andL.
kempii; Fig. 2). On the opposite extreme, group c included
the two highly oceanic species sharing the Type 3 life-cycle
pattern (D. coriacea,L. olivacea), but it also included one species
with the Type 2 life-cycle pattern (L. kempii). A third group
(b) was intermediate and contained mainly Type 2 species,
with the addition of L. olivacea. It is noteworthy that the
two Lepidochelys species are more similar to each other than
to the other species in their respective life-cycle pattern
groups.
This imperfect congruence between life-cycle patterns and
species average δ13C values indicates far greater complexity
in spatial foraging strategies within and among marine turtle
species. Indeed, when the intraspecific and interspecific
variation in δ13C values is viewed simultaneously, the spatial
foraging strategies of marine turtles are clearly seen as a
continuum (Fig. 5). Hence, the general life-cycle pattern
classification (Fig. 2) obscures fine-scale differences in spatial
habitat use among and within species, even within the same
macrohabitat foraging group.
In contrast to the congruence of spatial habitat use and
δ13C values, trophic level, estimated by δ15 N, is not likely
to be predicted cleanly from trophic morphology. This is
because, within a given trophic morphology, species are
expected to feed across trophic levels (Bjorndal, 1997). For
instance, D. coriacea, a specialized gelativore, feeds on both
primary consumers such as filter-feeding tunicates, but also
on carnivorous Cnidarians such as Portuguese man ‘o war
(Physalia physalis) and lion’s mane (Cyanea capillata), both of
which are known to feed on fish and which are thus at
least tertiary consumers (Paladino & Morreale, 2001). In the
case of C. caretta, a specialised durophage, stomach content
analyses indicate that it feeds on both low-trophic-level,
filter-feeding molluscs, and high-trophic-level, carnivorous
crustaceans (Plotkin, Wicksten & Amos, 1993). By contrast, C.
mydas, whose trophic morphology is specialised for herbivory,
is expected to forage only as a primary consumer.
Our analyses revealed four foraging groups (a–d) that
overlapped among species (Fig. 4D). Group a contains
Chelonia mydas and E. imbricata; group b contains E. imbricata,
C. caretta,andL. kempii; group c contains C. caretta and L.
olivacea; and group d contains L. kempii,L. olivacea and D.
coriacea.
Although there were four different groups with respect
to δ15N values, there was broad interspecific overlap in
trophic level. As a general rule of thumb, the discrimination
factor from diet to consumer is ∼3–4‰, representing one
trophic level (DeNiro & Epstein, 1981; Seminoff et al., 2009,
2006). Taken together, our analyses of δ13Candδ15N
values revealed that the trophic ecology of marine turtles
is not as typological as has long been hypothesised based on
life-cycle patterns (Fig. 2) and trophic morphology (Fig. 3).
While marine turtles exhibit some ecopartitioning of the
marine realm, the patterns are far more complex owing
to the substantial interspecific overlap of both their δ13C
and δ15N values, and to tremendous intraspecific variation
(Fig. 5). We now explore this intraspecific variation across
the hierarchical levels described in Fig. 1.
(2) Variation in trophic ecology among populations
In addition to the interspecific comparisons described above,
our data set affords the most complete picture to date of
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14 Christine Figgener and others
intraspecific and inter-population variation within each of
several species (B in Fig. 1). However, it is possible that
variation that might be ascribed to intraspecific variation
in trophic ecology is really due to differences among
basins in baseline isotope values (particularly 15N) which
have been hypothesised to exist (McMahon, Hamady, &
Thorrold, 2013; West et al., 2009, but see Pethybridge et al.,
2018). Hence, we attempted to account for basin effects in
several ways.
First, the nested ANOVAs that held tissue constant while
testing for species differences within three ocean basins
(Table S4b, d) revealed a basin effect on δ13C values, but not
on δ15N values. Second, examination of the scatterplot of
mean δ13Cversus δ15 N values (Fig. 5) reveals that values
are not clustered by basin within species as would be
expected if basin had an overriding effect. Rather it can
be seen that high and low values within a species are often
found within the same basin. Third, an additional ANOVA
nesting basins within species showed no basin effect for
δ15N values (Table S5d). Finally, we also attempted to adjust
for inter-basin differences in baseline levels of 15N using
phytoplankton baseline δ15N values extracted from a recent
study (Pethybridge et al., 2018) (see Table S6, Fig. S3). This
analysis did not materially alter the pattern shown in Fig. 5.
Taken together, this lack of inter-basin differences within
these species indicates that the trophic ecology of a given
species is not overly influenced by hypothesized differences
among ocean basins in baseline δ13Candδ15 N values (West
et al., 2009; McMahon et al., 2013). A pattern of relatively
similar 15N baseline levels across ocean basins, and ocean
regions within basins has also been documented in a recent
study of tuna species (Pethybridge et al., 2018). Hence, we
proceeded to evaluate intraspecific variation in isotope values
as being truly reflective of species trophic ecology rather than
being an artefact of basin effects.
The picture that emerges is that species exhibit tremendous
intraspecific variation as evidenced by a broad range of δ15N
values among populations for each species within each basin
(Figs S2d, S3). Given that a discrimination factor of 3–4‰
is typically regarded as representing one trophic step (see
Section I), it can be concluded that most species forage
across two or more trophic levels. Of the species for which
sufficient data exist (Table 2, Figs 5, S3), one species, L.
olivacea, is likely to forage at only a single trophic level
(Figs 5, S3). Two species, C. mydas and E. imbricata,are
likely to forage at two trophic levels. SIAs have revealed
cryptic diets in adult C. mydas with some populations being
clearly omnivorous and others herbivorous, in contrast to
the longstanding view that there is an obligate ontogenetic
dietary shift from omnivory to herbivory resulting in adults
being specialist herbivores (Hancock et al., 2018; Hatase
et al., 2006, Figs 5, S3). Two species, D. coriacea and C. caretta,
span more than two trophic levels between populations.
Hence, δ15N values reveal not only more interspecific
overlap than predicted from trophic morphology (see
Section IV.1), but also considerable intraspecific variation
in realised trophic levels not predicted by diet and trophic
morphology.
Our conclusions regarding the causes of inter-population
differences are rather different from those drawn
from single-species case studies. Six studies have
explored intraspecific differences in trophic ecology among
geographically distinct populations of the same life stage.
Four studies compared stable isotope ratios between
conspecifics within the same life stage inhabiting different
ocean basins: among C. caretta oceanic juveniles (Pajuelo
et al., 2010) and stranded juveniles, subadults, and adults
(Tomaszewicz et al., 2015); among D. coriacea oceanic adults
(Wallace et al., 2006); and among E. imbricata of unreported
life stage (Moncada et al., 1997). Two additional studies
examined differences among populations of C. caretta and C.
mydas within the same ocean basin (Vander Zanden et al.,
2013a; Cardona et al., 2014).
Two of the between-basin studies concluded that there is a
basin effect whereas the other two did not. Pajuelo et al. (2010)
and Wallace et al. (2006) found no differences in δ13C values
in either C. caretta or D. coriacea, respectively, between two
ocean basins. This similarity in carbon isotope ratio validates
each species’ inherent spatial foraging strategy, i.e. that they
utilise the same macrohabitat in each basin. Both of these
studies observed significantly enriched δ15N values in samples
from the eastern Pacific. A difference in nitrogen isotope
ratio typically indicates differences in trophic levels, but both
studies present evidence that these observed differences might
reflect differences in nitrogen-cycling processes between the
Atlantic and the eastern Pacific, rather than differences in
trophic level.
By contrast, the study comparing different life stages C.
caretta in the Atlantic and Pacific found higher δ13C values in
the Atlantic, which was interpreted as reflecting differences
in the spatial foraging strategy likely related to an ontogenetic
switch (Tomaszewicz et al., 2015). They found no difference
in δ15N values between the two ocean basins. Examination
of stable isotope patterns among different populations of E.
imbricata in the western Pacific, southeastern Indian Ocean,
and the Caribbean revealed higher δ13C values and lower
δ15N values in the Caribbean population than in populations
in the two other basins (Moncada et al., 1997). The authors
concluded that the δ13C values of the Caribbean population
reflect a closer dependency on coral reefs, and the high δ15N
values in the Pacific and Indian Ocean populations indicate
a diet containing more non-coral animal protein.
Two studies that have compared stable isotope
composition between populations within the same ocean
basin concluded that there are inter-population differences
within basins. The two studies examined the differences in
isotopic niches among populations of C. caretta (Cardona et al.,
2014) and C. mydas (Vander Zanden et al., 2013a) within the
same ocean basin. In C. caretta in the Mediterranean, stable
isotope composition represented a continuum that aligned
with different foraging areas and their respective productivity
levels. Oceanic currents and distance from the nesting
beaches were hypothesized to be the drivers of the differences
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Beyond Trophic Morphology 15
in foraging areas among populations (Cardona et al., 2014).
In C. mydas in the Caribbean, analyses revealed higher δ15N
values in adult nesting females in Costa Rica compared
to their foraging counterparts in Nicaragua, indicative of
a potential omnivorous diet. Further investigations using
amino acid-compound specific isotope analysis (AA-CSIA)
revealed that the differences in stable isotope composition
could be interpreted as a result of regional differences in
primary production and differences in nutrient cycling,
rather than evidence for an alternative foraging strategy
between different populations (Vander Zanden et al., 2013a).
The contrasting conclusions drawn from our meta-analysis
compared to these single-species case studies concerning
inter- or intra-basin differences in baseline isotope values
highlights the interpretive limitations inherent in two-sample
comparisons (Garland & Adolph, 1994). For example, a
comparison of point samples from a single population in each
basin could reflect basin differences (interpretations that have
been made) but also differences in local conditions, which are
not necessarily representative of the basin as a whole. While
it is tempting to ascribe an observed difference to one possible
cause over another in such comparisons, a two-sample design
does not permit such a distinction. For instance, several
studies compared an eastern Pacific sample to an Atlantic
sample. However, the eastern Pacific is substantially enriched
in 15N compared to several other regions of the Pacific
(Pethybridge et al., 2018), and hence is not representative
of the mean value in this basin. Because our meta-analysis
includes numerous observations from different regions in
each of several basins, our analyses (Tables 2,3, S4, S5, S6)
yielded estimates of within-basin variance that serve as a
quantitative basis for between-basin comparisons. In other
words, we were able unambiguously to test the hypothesis
that basins do not differ in their baselines, while accounting
for any within-basin variance that could obscure a true signal
of variation in trophic ecology. Thus, our findings urge
caution for future studies when interpreting heterogeneity
in stable isotope values when the sampling design does not
permit robust attribution among putative causes.
(3) Variation in trophic ecology within populations
(a)Variation in trophic ecology among life stages
Complex life cycles are characterised by abrupt changes in
trophic behaviour and habitat use, which result in shifts
in trophic niche (Wilbur & Collins, 1973; Wilbur, 1980;
Werner, 1988). This complexity is amplified in long-lived
organisms, which must balance an energetic trade-off
between maximising growth rates to minimise the time to
maturity while minimising predation risk (Werner & Gilliam,
1984). This trade-off often arises because different habitats
vary in their productivity, which in turn influences local
growth rates and time to maturity, but predation pressure
is typically greatest in more productive habitats (Werner &
Hall, 1988; Werner & Anholt, 1993). Body size throughout
ontogeny plays a major role in resolving this trade-off,
because of its large influence on an organism’s energetic
requirements and ability to exploit resources, but also its
susceptibility to natural enemies (Werner & Gilliam, 1984;
Werner & Hall, 1988; Werner & Anholt, 1993). It can also
be a factor in reducing resource competition between life
stages (Wilbur, 1980; Werner & Gilliam, 1984).
Not surprisingly, the complex life cycles and longevity
of marine turtles produce complicated patterns of habitat
use and trophic ecology across ontogeny (C.1 in Fig. 1). This
complexity arises due to both a progression of sizes (hatchlings
grow more than two orders of magnitude before attaining
maturity), and age-associated differences in form, function,
and ecology (different life stages use different macrohabitats;
Fig. 2).
There is a persistent knowledge gap concerning the habitat
use and specific spatial trophic ecology of early life-history
stages in turtles because they are hard to observe directly.
Before the use of SIA, knowledge of ontogenetic patterns
in the trophic ecology of early life stages was derived
from studies using methods such as mark–recapture and
gut-content analysis (Bjorndal, 1997). Such studies provided
the initial evidence for an ontogenetic shift from oceanic to
neritic habitat, thus establishing the existence of the Type
2 life cycle (Fig. 2). Yet it has remained difficult to pinpoint
the size class or age at which the transition from oceanic to
neritic feeding habitats occurs. Additionally, in the case of C.
mydas the gut-content approach revealed a shift in diet from
carnivory to herbivory, across a certain body-size threshold
(Bjorndal & Bolten, 1988; Bjorndal, 1997; Bolten, 2003). As
an example, Bjorndal & Bolten (1988) detected a shift from
oceanic to neritic habitats at 20–25 cm curved carapace
length (CCL) in C. mydas in the northwestern Atlantic using
repeated measurements of individuals and morphometric
analysis. These findings of ontogenetic niche shifts raise two
specific questions about the trophic ecology of different life
stages. The first concerns the timing (and size) of the predicted
transition from oceanic to coastal areas. The second concerns
the composition of diet (possibly cryptic) and trophic level of
individuals at a given life stage.
Stable isotopes have provided a powerful tool to address
these questions about habitat use and diet composition of
marine turtle early life stages. By analysing stable isotopes in
inert tissues (i.e. bone or scute layers), resampling individuals
multiple times, or combining SIA with skeletochronology,
SIA permits assessment of an individual’s foraging history
over multiple years or even its entire life. To date, 46 studies
have investigated ontogenetic differences in habitat and diet
in C. caretta (N=16), C. mydas (N=29), D. coriacea (N=1),
E. imbricata (N=2), L. kempii (N=1), and L. olivacea (N=2)
(Table S3).
Several stable isotope studies have addressed the question
concerning the timing of ontogenetic shifts from oceanic to
neritic habitat. One approach has been to examine stable
isotope values in different bone growth layers and translate
this into an estimation of size classes in C. caretta (Snover et al.,
2010) and C. mydas (Howell et al., 2016; Velez-Rubio et al.,
2016). Yearly somatic growth is recorded in annual marks in
humeri cross sections, and a transition from narrow growth
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16 Christine Figgener and others
marks to wider growth marks indicates a sharp increase in
growth rates and a potential shift from oceanic to neritic
habitats. SIA of the different layers corroborates a habitat
shift congruent with pelagic versus benthic feeding, and the
number of annual growth marks reveals the age at which the
habitat shift occurred.
A second approach has been to attempt to transform
size classes into age estimates. In north-eastern Atlantic
C. caretta, two studies estimated the shift to occur with
a straight carapace length (SCL) of about 54–55 cm, at
∼12 years of age (Avens et al., 2013; Ramirez et al., 2015). In
Atlantic C. mydas, Reich, Bjorndal, & Bolten (2007) estimated
the transition from oceanic to neritic habitats to occur at
3–5 years, at ∼25 – 35 cm SCL. To date, no stable isotope
studies have examined habitat shift in L. kempii, the most
endangered marine turtle species.
SIAs have corroborated the initial findings of an
ontogenetic habitat shift and have provided age estimates.
However, SIA has also revealed greater complexity than
was previously appreciated. One new insight is that the
behavioural flexibility required to shift habitats appears to be
confined to immature stages. Once maturity is attained,
adults seemingly have a diminished capacity to switch
foraging habitat preferences (oceanic versus neritic), even
if they are using a habitat that is sub-optimal in resource
abundance (Cardona et al., 2017). A second insight gained
from recent SIA is that there is inter-individual variation
among juveniles within a single population in the timing
and rapidity of such transitions (Ramirez et al., 2015). Some
juveniles shift quickly and discreetly (within a year), while
shifts in others are more protracted (up to 5 years) and
happen in increments. Further, in some populations juveniles
also display a recurrent seasonal (winter versus summer) shift
between neritic and oceanic foraging habitats (McClellan
et al., 2010). Further, some individuals never shift and remain
in the oceanic habitat (Cardona et al., 2017). Finally, several
studies have demonstrated between-population variation in
use of oceanic and neritic foraging grounds in both C. caretta
(Casale et al., 2008; McClellan et al., 2010) and C. mydas
(Hatase et al., 2006; Araujo Morais et al., 2014).
There are multiple reasons why marine turtles do not
remain in one developmental habitat until they reach
maturity. Complex life-cycle theory postulates that different
habitats utilised for foraging by different life stages play
an important role in growth and maturation and might
obviate intraspecific competition between life stages (Wilbur
& Collins, 1973; Werner, 1988). In marine turtles, the
open ocean provides protection from predators and thermal
refuges for small size classes associated with floating Sargassum
(Witherington, Hirama & Hardy, 2012). Also, predator
densities are lower in the open ocean (Carr, 1987; Bolten,
2003). However, there will be a trade-off with slower growth
rates in oceanic habitat because productivity is lower than in
coastal areas. Once a size refuge from predation is attained,
juveniles can exploit the more productive coastal foraging
areas, which accelerates growth (Bolten, 2003).
The second question that SIA has illuminated regards
ontogenetic shifts in diets, such as trophic level and dietary
composition (e.g. herbivory versus carnivory), which are
unrelated to changes in spatial habitat use (shift from oceanic
pelagic prey to neritic benthic prey). Four studies have
investigated this question in C. caretta in Atlantic and Indian
Ocean populations (Wallace et al., 2009; McClellan et al.,
2010; Thomson et al., 2012; Hall et al., 2015); 19 studies
in Atlantic C. mydas (Burgett et al., 2018; Cardona et al.,
2009b; Di Beneditto, Siciliano & Monteiro, 2017; Gillis et al.,
2018; Gonzales Carman et al., 2014; Hancock et al., 2018;
Howell et al., 2016; Velez-Rubio et al., 2016; Williams et al.,
2014), Pacific C. mydas (Arthur, 2008; Barcel´
o, 2018; Lemons
et al., 2011; Prior, Booth & Limpus, 2015; Rodríguez-Bar´
on,
2010; Sampson et al., 2017; Santos-Baca, 2008; Shimada
et al., 2014), and C. mydas in the Indian Ocean (Burkholder
et al., 2011) and in the Mediterranean (Cardona et al., 2010);
one study in Atlantic D. coriacea (Wallace et al., 2014), one
study in E. imbricata (Ferreira et al., 2018), and one study in
L. olivacea (Peavey et al., 2017).
No differences in diet and trophic level among life stages
have been detected in stable isotope ratios of C. caretta despite
several attempts to find them (Wallace et al., 2009; McClellan
et al., 2010; Thomson et al., 2012; Hall et al., 2015). The only
differences were those congruent with the already mentioned
spatial habitat shift and a resulting increase in trophic level
with body size when shifting from pelagic to benthic prey.
The overall pattern indicated by SIA of C. caretta is that
observed changes in stable isotope compositions are based
solely on the transition of juveniles between macrohabitats
rather than on a change in trophic level (McClellan et al.,
2010; Hall et al., 2015).
By contrast, in D. coriacea an increase in δ15N values with
increasing body size was detected among life stages (Wallace
et al., 2014) and in E. imbricata data showed that immature
life stages occupy a significantly smaller isotopic niche than
adults, but no difference in trophic level was found (Ferreira
et al., 2018). Several SIA studies of C. mydas from multiple
ocean basins indicate a general pattern of ontogenetic dietary
shift to a lower trophic level with increasing body size: from
carnivory or omnivory to herbivory with increasing body
size. For example, Velez-Rubio et al. (2016) documented a
relationship between diet (a shift between omnivory and
herbivory) and body size (gelatinous macrozooplankton
in turtles <45 cm CCL, and predominantly herbivory in
individuals >45 cm). Another study found a similar pattern,
but at a larger body size (CCL >59 cm) (Cardona, Aguilar
& Pazos, 2009a). These findings corroborate earlier work
based on gut-content analyses indicating a transition from
omnivory in early life stages to strict herbivory in adults
(Bjorndal, 1997). However, a study in an eastern Pacific
population did not find differences in diet between adults
and immature stages suggesting a lack of ontogenetic dietary
shift and that adults remained omnivores (Lemons et al.,
2011). Studies in the western Pacific and eastern Atlantic
found a similar pattern (Shimada et al., 2014; Hancock et al.,
2018). Further, one study detected an asynchronous shift
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Beyond Trophic Morphology 17
between diet and which dietary components constitute the
main nutritional source (protein versus plant matter) (Cardona
et al., 2010). A high-protein diet derived from carnivory fuels
the growth of early life stages, thus minimising time to
maturity and attainment of a size refuge from predation
(Werner & Gilliam, 1984; Werner, 1988; Werner & Hall,
1988; Werner & Anholt, 1993). Additionally, several studies
found regional differences (Prior, Booth, & Limpus, 2015;
Gillis et al., 2018) and inter-individual differences in diet
within the same life stage (Barcel´
o, 2018; Burgett et al.,
2018).
(b)Variation in trophic ecology between sexes
The next hierarchical level at which a species may mitigate
intraspecific competition is between sexes of adult individuals
(C.2 in Fig. 1). This question has barely been investigated
in marine turtles, which reflects a persistent knowledge gap
concerning male biology and ecology because of a research
bias towards studying nesting females. Only seven studies
to date have investigated intersexual differences in trophic
ecology: C. caretta in the Atlantic (Pajuelo et al., 2016, 2012),
D. coriacea in the Atlantic (Dodge, Logan & Lutcavage, 2011;
Wallace et al., 2014), C. mydas in the Atlantic and in the
Pacific (Vander Zanden et al., 2013a; Prior et al., 2015), and
L. olivacea in the Pacific (Peavey et al., 2017).
Only one study detected significant intersexual differences
in stable isotope composition, particularly in δ13C, in D.
coriacea (Dodge, Logan, & Lutcavage, 2011). These data
suggest differences in spatial foraging patterns, which could
be the result of divergent migratory cycles between male
and female D. coriacea that reside for different time intervals
in northern foraging areas (James, Eckert, & Myers, 2005a;
James, Myers & Ottensmeyer, 2005b), with males spending
annually extended periods in tropical, coastal areas adjacent
to nesting beaches, and females foraging for 2–3 years in
northern oceanic habitat. The study found elevated female
δ13Candδ15 N values compared to males, which suggests that
females forage closer to the coast or at lower latitudes than
males (Kelly, 2000; Rubenstein & Hobson, 2004). However,
the reverse pattern should be expected for male and female
stable isotope ratios according to their divergent migratory
cycles. An alternative explanation could be that the energetic
demands of nesting (migration, egg production, starvation
during nesting season) and the resulting nutritional stress
cause elevated δ13Candδ15N values in females (Hobson,
Alisauskas & Clark, 1993).
By contrast, all other studies comparing male and female
trophic ecology did not detect any isotopic differences in
either spatial foraging patterns or trophic level. The most
plausible explanations for this is that first, both sexes of
marine turtles exhibit natal philopatry and it is likely that
they will also share the same developmental habitats and
later on foraging habitat. Further, they exhibit very little
sexual size dimorphism (Figgener, Bernardo & Plotkin, 2018)
compared to other turtle species (Abouheif & Fairbairn,
1997; Agha et al., 2018; Berry & Shine, 1980; Bonnet et al.,
2010; Ceballos et al., 2013; Gosnell, Rivera & Blob, 2009;
Hal´
amkov´
a, Schulte & Langen, 2013), or species where
strong size dimorphism aligns with divergence in trophic
morphology and ecology (e.g. lizards and bird-eating hawks
(Schoener, 1967, 1984). Lastly, the energy expenditures
between the two sexes are similar and would not suggest a
difference in diet or trophic level. Female marine turtles bear
the energetic expenditure of egg production, however in most
species (excepting Lepidochelys spp.) females counterbalance
these expenditures by skipping nesting seasons to forage
for extended periods (Limpus, 1993; Miller, 1997; Plotkin,
2003; James, Myers, & Ottensmeyer, 2005b), whereas males
migrate to breeding sites adjacent to nesting beaches annually
(Limpus, 1993; James et al., 2005a;Hayset al., 2010).
While most of the available data indicate no differences
in male–female trophic ecology, this conclusion should
be viewed as tentative, given the dearth of data and
that differences in migratory timing between sexes (males
spending time annually in coastal, neritic areas), in
combination with the protracted integration times of stable
isotopes into tissues, could result in differences in at least
δ13C values. Future studies of multiple populations of
multiple species should attempt to integrate male–female
comparisons.
(4) Variation in trophic ecology among adults
within a population and its effect on individual
fitness
The last hierarchical level at which intraspecific competition
might be ameliorated is among individuals irrespective of
ontogenetic stage and sex (D in Fig. 1). This level of variation
is surprisingly understudied, although it is an emerging
theme in recent literature (Bolnick et al., 2003; Araujo,
Bolnick, & Layman, 2011; Violle et al., 2012). Interestingly,
this question has been studied extensively in adult marine
turtles using SIA: 41 studies have investigated variation
in trophic ecology among individuals within populations
for six species and two ocean basins (Table S3). The two
main patterns emerging from these SIA studies are first
that most populations comprise two or three subgroups that
exhibit consistent associations with geographically distinct
foraging areas and second, that populations exhibit high
inter-individual variation in trophic ecology.
The first pattern typically involves a spatial subdivision
of adults foraging in either highly productive or
low-productivity habitats. This dichotomy often aligns
either with neritic versus oceanic foraging areas (Eder et al.,
2012; Hatase, Omuta & Tsukamoto, 2010; Hatase, Omuta
& Tsukamoto, 2013; Hawkes et al., 2006; Lopez-Castro
et al., 2013; Robinson et al., 2016; Watanabe et al., 2011)
or high- versus low-latitude foraging areas (Ceriani et al.,
2012). Interestingly, L. olivacea,whichisknownforits
long-distance, nomadic migrations (Plotkin, 2010), does not
show a dichotomy between individuals feeding in high- or
low-productivity habitats (Dawson, 2017; Peavey et al., 2017;
Petitet & Bugoni, 2017). The presence of divergent spatial
foraging strategies within populations and the exact patterns
vary among the species and populations examined. But
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18 Christine Figgener and others
divergent spatial foraging strategies have been recorded in
populations of four out of six studied species (C. caretta,C.
mydas,E. imbricata,andD. coriacea).
Although a dichotomous foraging strategy within a
population is common in some species of marine turtles, its
underlying mechanisms are barely studied. One attempt to
determine whether foraging dichotomies have a genetic basis
concluded that they are the result of phenotypic plasticity
cued by early growth rates (Hatase, Omuta, & Tsukamoto,
2010; Watanabe et al., 2011). An understanding of the causes
of divergent foraging strategies warrants further examination.
An observation made by several studies is that individuals
foraging in more productive areas (e.g. neritic) tend to have a
larger body size compared to those foraging in less-productive
areas (Hatase et al., 2002; Eder et al., 2012; Lontoh, 2014;
Vander Zanden et al., 2014a; Patel et al., 2015). Additionally,
in northeastern Atlantic C. caretta, data indicate that head
size in adults is related to preferred foraging areas and not
to trophic level and is only to a small degree explained by
variation in body size (Price et al., 2017).
There have been several attempts to evaluate the
implications of foraging dichotomies on fitness. The
most comprehensive effort to date examined the foraging
dichotomy (neritic versus oceanic) among sympatrically
nesting C. caretta in the Western Pacific detected using SIA
(Hatase, Omuta, & Tsukamoto, 2013). Using a remarkable
long-term data set of 26 years, the authors analysed variation
in different life-history traits and found significant differences
between the two foraging groups in body size, clutch
size, clutch frequency, breeding frequency, and remigration
intervals. Using this information they computed cumulative
reproductive output (total number of emerged hatchlings
produced per female) of the two foraging groups and found
a significant difference between foraging groups, with neritic
feeders having a 2.4-fold larger reproductive output. Several
other studies of C. caretta (Hatase et al., 2002; Eder et al., 2012;
Cardona et al., 2014; Vander Zanden et al., 2014a; Patel et al.,
2015;Ceriani et al., 2017) and D. coriacea (Lontoh, 2014) also
investigated this question, but with short-term data (usually
a single nesting season) and only for a few traits (usually
body size and clutch size). All of these studies detected
similar life-history differences between individuals using
high- versus low-productivity foraging areas. Although these
findings are congruent with Hatase et al.’s (2013) findings
that individuals using high-productivity foraging areas have
higher fitness than individuals feeding in low-productivity
areas, these other studies should be viewed as preliminary
because they only represent snapshots of fitness components.
Robust conclusions that the dichotomous foraging strategies
that have been repeatedly identified using SIA translate into
fitness consequences can only be drawn with long-term data.
The compelling finding of apparent fitness differences
between foraging groups (Hatase et al., 2013) raises the
further question of whether a trade-off exists that balances
fitness between the two strategies, therefore maintaining
both within a single population. To address this question
numerous traits including age (Hatase et al., 2010), egg
size & components (Hatase, Omuta & Komatsu, 2014),
hatchling size (Hatase, Omuta & Komatsu, 2015) and various
traits presumed to be indicative of offspring quality (Hatase
et al., 2018) have been investigated that might contribute to
such a trade-off. None of these studies revealed a fitness
trade-off. A robust way to evaluate the fitness effects of
divergent life-history strategies is a life-table approach, which
can mathematically determine whether alternative strategies
produce equivalent fitness (Tilley, 1980). This approach
requires age-specific data on onset of reproduction, fecundity,
survivorship, and the duration of the reproductive lifespan.
Such analyses are not currently feasible for marine turtles
because of a lack of suitable data for a single species, let
alone for the divergent population-level foraging subgroups
identified by SIA.
The second emerging pattern is that many populations
show high inter-individual variability that does not align
with geographically distinct foraging areas. Although 61%
of the available studies concern C. caretta, this pattern has
been identified in four out of six species studied (C. caretta,
C. mydas,L. kempii,L. olivacea) and aligns with the findings
of our meta-analysis (Section IV.1). Often individuals within
a population are more specialised, that is, individuals have
a narrower isotopic niche width than the average isotopic
niche width of the population or species would suggest
(Pajuelo et al., 2016; Peavey et al., 2017; Petitet & Bugoni,
2017; Reich et al., 2017; Vander Zanden, Bjorndal & Bolten,
2013b; Vander Zanden et al., 2010).
Further, where studied, this among-individual
sub-specialisation in adults is persistent through time
(Pajuelo et al., 2016; Vander Zanden, Bjorndal, & Bolten,
2013b, 2010). These chronological records have been
obtained by either looking at annual growth layers in bone
or scute tissue, or by resampling of recaptured individuals
over time. For instance, Vander Zanden et al. (2010) detected
long-term specialisation in resource use of individual C.
caretta by examining stable isotope composition across
numerous scute layers reflecting up to 12 years of foraging
history. Thus marine turtles add to the growing literature
that demonstrates that generalist animal species are often
composed of ecologically heterogeneous individuals that
repeatedly differ in foraging behaviour and use different
subsets of the available resources (Bell, Hankison &
Laskowski, 2009; Bolnick, Svanback & Araujo, 2007a;
Bolnick et al., 2003).
These studies provide evidence for higher intraspecific
variation in the exploitation of the trophic axis than
previously recognised, thus indicating that individualism is
an important component of marine turtle trophic ecology.
V. DISCUSSION
This systematic review was motivated by the lack of synthesis
of marine turtle stable isotope data to achieve a more
in-depth view of their ecology and evolution. This exercise
revealed far greater complexity in trophic ecology within
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Beyond Trophic Morphology 19
and among species than previously hypothesised. These
findings inform marine turtle ecology, conservation and
management, elucidate the ecological role of marine turtles
in the marine realm, and have much broader implications
for the study of ecological radiations.
(1) Novel insights about marine turtle trophic
ecology from stable isotope analysis
Marine turtles are widely distributed throughout all ocean
basins and inhabit diverse ecosystems, and it has long been
appreciated that they show a clear interspecific signature of
ecopartitioning of the marine realm and are highly diversified
in life-history traits and ecology (Hendrickson, 1980; Van
Buskirk & Crowder, 1994; Bjorndal, 1997; Bjorndal &
Jackson, 2002; Bolten, 2003). They show particularly striking
variation in trophic morphology, which is evident among
both extant species (Fig. 3) and throughout the rich fossil
record spanning more than 120 million years (Kear & Lee,
2006; Parham & Pyenson, 2010; Cadena & Parham, 2015;
Gentry, 2017).
Despite these long-standing qualitative characterisations of
variation in marine turtle trophic ecology, our meta-analysis
of interspecific variation in isotopic composition is the
first quantitative assessment of the hypothesis that they do
partition marine resources, and the extent to which species
differ (Figs. 4,5, S2). Our quantitative analysis corroborates
previous but incomplete qualitative evidence from variation
in trophic morphology, microhabitat use and gut-content
analyses that marine turtles exhibit ecopartitioning of
resources. No prior study has performed any quantitative
statistical assessment of this hypothesis, in part because
neither quantitative characterisation of trophic morphology,
nor of habit use, nor of gut contents across all species has
ever been published.
Additionally, our review revealed a continuum of trophic
sub-specialisation in most species, which extends beyond
interspecific differences and ranges from variation in trophic
niches between populations of the same species in different
ocean basins and geographic regions, to variation of trophic
niches among life stages and individuals within populations
(Fig. 1). This ubiquity of trophic sub-specialisation at many
levels exposes a far more complex view of marine turtle
ecology and resource-axis exploitation than is suggested by
species diversity alone.
While our review has demonstrated the power of SIA
to elucidate many aspects of trophic ecology of marine
turtles, it has also revealed substantial research gaps. These
gaps probably exist because most studies were typically
addressing narrower questions concerned with conservation,
usually focusing on a single species. In particular, we
note three major issues. First, while most species occupy
multiple ocean basins (Table S1), there is uneven sampling
across ocean basins (Table S2) and regions within basins
(Figgener et al., 2019). For instance, only five studies have
been conducted in the Indian Ocean (Table S2) (Moncada
et al., 1997; Burkholder et al., 2011; Thomson et al., 2012,
2018; Robinson et al., 2016) and none in the Red Sea. This is
relevant because heterogeneity of biogeochemical processes
on both the basin and regional scales (Wallace et al., 2006;
Pethybridge et al., 2018) affects baseline values of δ13 Cand
δ15N, and populations are different in size and face different
intensities of threats.
The second issue is that sampling effort for each species is
uneven. For instance, there is a paucity of studies of L. kempii,
E. imbricata,andL. olivacea compared to C. caretta,C. mydas,
and D. coriacea and no studies for N. depressus (Table S2).
The third issue is that there is no common currency
or standardisation for sampled tissues across stable isotope
studies, hindering comparative analyses. Nearly a dozen
different tissues have been used in SIA of marine turtles
(Table 2 in Figgener et al., 2019), but tissues differ in
discrimination factors and turnover times (Reich et al.,
2008; Seminoff et al., 2009, 2006; Vander Zanden et al.,
2012, 2014b), which both influence stable isotope estimates.
Moreover, in most cases, there is no way to convert stable
isotope values of one tissue accurately into the values of
another (Ceriani et al., 2014; Vander Zanden et al., 2014b).
Hence, we suggest that future studies always include stable
isotope estimates from skin, a tissue easily sampled and
stored, which will facilitate future comparative analyses.
In conclusion, our comparative analysis indicates that the
longstanding idea that trophic morphology provides robust
insights into interspecific variation in foraging ecology is
incomplete, both with respect to marine turtles and possibly
in other vertebrate radiations as well. In other words, SIA
is a powerful tool to detect cryptic variation in trophic
ecology beyond trophic morphology, permitting a more
comprehensive understanding of ecological radiations and
food-web structure.
(2) Implications for marine turtle conservation
and management
The continuum of trophic specialisation both among and
within species of marine turtles revealed by our review has
several implications for conservation and management. First,
the ubiquity of this pattern adds another underappreciated
dimension to marine turtle conservation and management
beyond that informed by traditional genetically defined
management units. In particular, it is now clear that even
within management units marine turtle populations are
comprised of individuals using ecologically distinct strategies
and therefore are not ecologically exchangeable. Ecological
exchangeability refers to the idea that individuals can be
moved between populations and can occupy the same
ecological niche or selective regime (Crandall et al., 2000).
Under this idea, the null hypothesis is that two or more
populations of a species are ecologically equivalent, even if
they are genetically distinct.
Conversely, two or more populations that are ecologically
distinct are not ecologically exchangeable, even if they
are part of the same genetically defined management
unit. Numerous studies reviewed here show that the latter
is typically the case for marine turtles. This ecological
diversity within stocks necessitates a more comprehensive
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

20 Christine Figgener and others
management approach beyond the genetic stock concept,
which drives current understanding of management units.
Related to this issue is the fact that research effort across
genetically defined management units is uneven, and many
stocks are completely unstudied (Pearson et al., 2017). Hence,
there could be as-yet-unrecognised cryptic variation in
trophic ecology within these units.
Another consideration is that the two most geographically
restricted species are essentially unstudied with respect to
stable isotopes. Natator depressus, which is listed as data
deficient by the IUCN (Red List Standards & Petitions
Subcommittee, 1996), has yet to be studied, and there
are only two studies of L. kempii, one of the two most
endangered marine turtle species (Marine Turtle Specialist
Group, 1996; Plotkin, 2016). The insights concerning trophic
ecology (habitat use, trophic level) that would emerge from
SIA of these species would be an invaluable tool for their
conservation and management.
Another insight from our review is that SIA has revealed
previously unknown patterns of habitat use of early life
stages of marine turtles, which are poorly studied because
direct observations of foraging areas in the marine realm are
logistically challenging. For example, time series sampling
of humeri of stranded turtles (Tomaszewicz et al., 2016)
has yielded insights into ontogenetic patterns in trophic
ecology (Tomaszewicz et al., 2018, 2017b), yet few studies to
date have exploited this opportunity. Such insights would
facilitate the location of critical habitats for growth and
development of juveniles and subadults, potentially resulting
in more effective protective measures for these life stages
Additionally, locating hotspots of immature life stages would
likely increase our ability to study them directly using
mark–recapture and tracking studies to close longstanding
gaps in our understanding of marine turtle demography.
(3) Ecological roles of marine turtles in the marine
realm
The ubiquitous signal of ecological versatility among and
within marine turtle species revealed by our synthesis paints
a more complex picture of their ecological roles in the
marine realm than has previously been appreciated and
which is distinct from those of other large, marine predatory
vertebrates. It is now widely documented that losses of
apex predators, including in marine systems, cause a wide
variety of down-web effects including trophic cascades and
general trophic downgrading of marine ecosystems (Pace
et al., 1999; Heithaus et al., 2008; O’Gorman & Emmerson,
2009; Estes et al., 2011), secondary extinctions (Borrvall &
Ebenman, 2006), altered biogeochemical cycles (Estes et al.,
2011), and regime shifts (Scheffer et al., 2001; Barnosky et al.,
2012). Like other large marine predatory vertebrates, all
species of marine turtles are of conservation concern, but the
justification for their conservation is largely driven by their
charismatic appeal rather than because of their ecological
role in marine ecosystems (but see Bjorndal & Jackson, 2002).
Perhaps the most remarkable finding to emerge from our
meta-analysis is that adults of four species of marine turtles
exhibit broad intraspecific trophic niches, foraging across
2–4 trophic levels among and within populations [C. caretta,
D. coriacea,E. imbricata,L. olivacea (Table 2, δ15 Naxison
Fig. 5; Figgener et al., 2019)]. This pattern is also evident
within a single study of a fifth species, L. kempii (Reich
et al., 2017). These broad trophic niches of marine turtle are
unlike those found in other marine predators. SIA of marine
predators as varied as squid (Navarro et al., 2013), bony
fishes (Torres-Rojas et al., 2014; Pethybridge et al., 2018),
sharks (Estrada et al., 2003; Hernandez-Aguilar et al., 2016),
and cetaceans (Abend & Smith, 1997; Hooker et al., 2001;
Herman et al., 2005) consistently exhibit a narrow isotopic
niche indicating feeding at a single, usually high, trophic
level. What is even more remarkable is that this pattern of
feeding across multiple trophic levels occurs in three species
that otherwise exhibit trophic specialisations for certain types
of prey –D. coricaea (gelativory), C. caretta (durophagy) and
E. imbricata (spongivory). Thus, marine turtle species span a
broader ecological continuum in the oceans far beyond that
suggested by their well-established trophic ecomorphology,
showing a ubiquitous ecological versatility.
This ecological versatility is also evident intraspecifically,
both across ontogeny and among individuals (Fig. 1).
Although these questions have only been addressed in
two species (C. caretta and C. mydas), several insights have
emerged. Where studied, juveniles appear to be more
flexible in their dietary choices and foraging habitat use,
whereas adults are typically consistent in both respects
through time (Section IV.3aand IV.4). A second insight
is that oceanic and neritic juveniles exhibit less individual
specialisation in trophic ecology than adults. Additionally,
in some species, adults exhibit different but individually
consistent foraging strategies, thus resulting in a generalist
population with individual specialists. Thus, both ontogenetic
variation and individuality in foraging strategies expand the
trophic footprint of marine turtles. Analysis of ontogenetic
and inter-individual variation in trophic ecology of other
species is likely to be a fruitful area for future research.
Taken together, the inter- and intraspecific signal of
marine turtle feeding across numerous trophic levels indicates
a complex interconnectedness with an influence upon marine
food webs. Theoretical and empirical studies of food-web
connectedness generally indicate that such multilevel trophic
interactions act to stabilise food webs (Dunne, Williams &
Martinez, 2002; O’Gorman & Emmerson, 2009; Th´
ebault
& Fontaine, 2010), buffering their dynamics against species
gains and losses. By contrast, food webs tend to become
destabilised when species that feed on a single trophic
level are gained or lost. For example, losses of apex
predators have been shown to produce trophic cascades
across both aquatic and terrestrial ecosystems (Pace et al.,
1999; Heithaus et al., 2008; O’Gorman & Emmerson, 2009;
Estes et al., 2011; Ripple et al., 2014) and in the extreme, may
result in down-web extinctions (extinctions at lower trophic
levels) (Borrvall & Ebenman, 2006; Sanders et al., 2018;
S¨
aterberg, Sellman & Ebenman, 2013). Hence, that marine
turtles feed across multiple trophic levels, both inter- and
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Beyond Trophic Morphology 21
intraspecifically, indicates that they likely have a stabilising
effect on food webs buffering trophic cascades that are elicited
by the removal of apex predators such as sharks (Heithaus
et al., 2008). This broader view of the ecological role of marine
turtles in the marine realm also provides a material argument
for their conservation beyond their charismatic appeal.
Additionally, this broad ecological role of marine turtles
indicates that they may be among the best sentinels of ocean
health, reflecting changes in baseline primary productivity
and nitrogen-cycling processes transferred through several
trophic levels (Wallace et al., 2006).
(4) Implications for future research on ecological
radiations
Although marine turtles are well-known subjects of
conservation efforts, their value as a model system for
understanding broader ecological and evolutionary questions
is underappreciated. In particular, the trophic complexity
within and among species revealed by our analyses suggests
that novel insights concerning resource partitioning in other
ecological radiations might arise from SIAs across the
hierarchical levels described in Fig. 1.
Since Darwin first remarked upon the striking variation in
trophic morphology among Geospiza finches (Darwin, 1839),
analyses of easily recognisable interspecific differences in
body size and sizes and shapes of trophic structures have
been the dominant theme in studies of ecological radiations
(Schluter, 2000; Streelman & Danley, 2003). This research
tradition has demonstrated that trophic morphology can
reliably predict some degree of interspecific ecopartitioning,
but it also has shown that ecopartitioning is often imperfect.
Because SIA is a measure of realised trophic ecology, it
gives a different and more comprehensive perspective on the
degree to which closely related species partition versus overlap
in resource use than trophic morphology alone. Some insights
that have emerged from SIA are broader trophic niches in
the case of aquatic insect ecomorphs (see Section I), and both
cryptic habitat use and diet breadth as we have shown here for
marine turtles. Thus, because the degree of overlap predicted
by trophic morphology underestimates the true breadth of
realised trophic niche, future studies of ecological radiations
would likely benefit from incorporation of SIA, advancing
beyond the singular consideration of trophic morphology.
VI. CONCLUSIONS
(1) Our contribution aimed to provide a quantitative
analysis of interspecific variation and a comprehensive review
of intraspecific variation in trophic ecology of marine turtles
across different hierarchical levels, marshalling insights about
realised trophic ecology derived from stable isotopes.
(2) 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 beyond interspecific differences. This ubiquity of
trophic sub-specialisation at many levels exposes a far more
complex view of marine turtle ecology and resource-axis
exploitation than is suggested by species diversity alone.
(3) Our findings are highly relevant to conservation man-
agement because they imply ecological non-exchangeability,
which introduces a new dimension beyond that of genetic
stocks which drives current conservation planning.
(4) The insight that marine turtles are robust sentinels
of ocean health and likely stabilise marine food webs has
broader significance for studies of marine food webs and
trophic ecology of large marine predators.
(5) The value of marine turtles as a model system
for understanding broader ecological and evolutionary
questions is underappreciated and our findings 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.
VII. ACKNOWLEDGMENTS
We would like to thank Tiffany Dawson for providing us her
unpublished data and Dr. Sterba-Boatwright for statistical
advice. We are further grateful to Texas A&M University
for providing summer support during the writing process.
We also thank two anonymous reviewers who provided
constructive comments.
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IX. SUPPORTING INFORMATION
Additional supporting information may be found online in
the Supporting Information section at the end of the article.
Table S1. A survey of studies documenting regional spatial
overlap of marine turtle species.
Table S2. Summary table showing the number of studies
using stable isotope analysis (SIA) of δ13Candδ15Nto
investigate the trophic ecology of marine turtles, organised
by species and ocean basin.
Table S3. Summary table showing the number of studies
using stable isotope analysis (SIA) of δ13Candδ15Nto
investigate the trophic ecology of marine turtles, organised by
species and broader study topic introduced in the conceptual
model shown in Fig. 1.
Table S4. Nested analyses of variance (ANOVAs) modelling
interspecific differences in stable isotope values taking
into account variation among sampled tissues and ocean
basins.
Table S5. Nested analyses of variance (ANOVAs) modelling
difference in stable isotope values among basins and tissues
taking into account variation among species.
Table S6. Summary statistics of unadjusted δ15Nand
adjusted δ15N values from 91 data points of adult marine
turtles used in our meta-analysis.
Figure S1. High-resolution version of the images shown in
Fig. 3.
Figure S2. Exploratory data analyses comparing values of
δ13Candδ15N among species within tissues within one
ocean basin (Atlantic, the basin with most estimates) (A, C)
and among species within ocean basins within one tissue
(skin, the tissue with most estimates) (B, D).
Figure S3. Scatterplot of 91 means from values of δ13C
and adjusted values of δ15N [adjusted using baseline
phytoplankton data extracted from Pethybridge et al., 2018,
see Table S6] in adults of six marine turtle species.
(Received 13 December 2018; revised 7 June 2019; accepted 13 June 2019 )
Biological Reviews (2019) 000– 000 ©2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.