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Direct Evidence for Gradual Ontogenetic Dietary Shift in the Green Turtle,Chelonia mydasAuthor(s): Renato Araujo Morais, Robson Guimarães dos Santos, Guilherme Ortigara Longo, EduardoTadashi Estevam Yoshida, Gustavo David Stahelin, , and Paulo Antunes HortaSource: Chelonian Conservation and Biology, 13(2):260-266. 2014.Published By: Chelonian Research FoundationDOI: http://dx.doi.org/10.2744/CCB-1058.1URL: http://www.bioone.org/doi/full/10.2744/CCB-1058.1

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Chelonian Conservation and Biology, 2014, 13(2): 260–266g 2014 Chelonian Research Foundation

Direct Evidence for Gradual OntogeneticDietary Shift in the Green Turtle,

Chelonia mydas

RENATO ARAUJO MORAIS1,2,

ROBSON GUIMARAES Dos Santos3,*,

GUILHERME ORTIGARA LONGO1,2,

EDUARDO TADASHI ESTEVAM YOSHIDA2,

GUSTAVO DAVID STAHELIN4, AND

PAULO ANTUNES HORTA1,5

1Programa de Pos-Graduacao em Ecologia, Universidade Federalde Santa Catarina, Florianopolis, SC, 88010-970, Brazil

[renatomoraisaraujo@gmail.com; golerme@yahoo.com.br;tadashivet@yahoo.com.br; phone: (5548) 3721-5521];

2Laboratorio de Biogeografia e Macroecologia Marinha, Centro deCiencias Biologicas, Universidade Federal de Santa Catarina,

Florianopolis, SC, 88010-970, Brazil;3Departamento de Oceanografia e Ecologia, Universidade Federal

do Espırito Santo, Vitoria, ES, 29075-910, Brazil[robsongsantos@gmail.com];

4Fundacao Pro-Tamar, Caixa Postal 5098, Trindade, Florianopolis,SC, 88040-970, Brazil [gustavo@tamar.org.br];

5Departamento de Botanica, Universidade Federal de SantaCatarina, Florianopolis, SC, 88040-900, Brazil

[pahorta@ccb.ufsc.br]*Corresponding author

ABSTRACT. – Here we provide information on the diet ofjuvenile green turtles from neritic developmentalhabitats in the South Atlantic that indicates the existenceof a gradual dietary shift from a primarily carnivorousto a primarily herbivorous diet. Linear regression show-ed a relation between the size of turtles (n = 22) and theproportion of vegetal matter in the diet, with smalleranimals being predominantly carnivorous. We propose 3hypotheses that could explain these observations.

Ontogenetic habitat shifts are widespread phenomena

well documented in marine species (Werner and Gilliam

260 CHELONIAN CONSERVATION AND BIOLOGY, Volume 13, Number 2 – 2014

1984; Snover 2008). These shifts are driven by different

combinations of potential factors such as predation risk,

competition, susceptibility to physical factors, and

maximization of growth rates (Werner and Gilliam

1984). Habitat shifts also affect patterns of resource use,

often resulting in a dietary shift due to shifts in prey

availability (Snover 2008).

The life history of marine turtles is an iconic example

of ontogenetic changes in habitat use (Arthur et al. 2008).

After emerging from their nests and reaching the sea,

hatchlings frenzy-swim from near-shore shallow waters

to the oceanic zone, where predation is assumed to be

lower (Wyneken and Salmon 1992). In the posthatchling

oceanic stage, marine turtles are epipelagic and omniv-

orous with a strong tendency to carnivory (Bjorndal

1985). After several years dwelling in the oceanic zone,

most sea turtle species shift to coastal habitats and, as a

result, major changes in behavior and resource use occur

(Bolten 2003; Arthur et al. 2008). However, some studies

have demonstrated that this habitat shift is not obligatory,

showing the existence of plasticity in the use of pelagic

and neritic foraging grounds among adults and juveniles

turtles (e.g., Casale et al. 2008; Hatase et al. 2006).

The green turtle, Chelonia mydas, is the only

herbivorous marine turtle primarily feeding on algae or

seagrass (or both; Bjorndal 1997). Recruitment to the

neritic zone occurs at curved carapace lengths (CCLs)

between 20 and 25 cm in the Northwestern Atlantic

(Bjorndal and Bolten 1988). This turtle’s neritic recruit-

ment involves what is believed to be an abrupt change in

its diet and foraging behavior from primarily carnivore to

a primarily herbivorous diet (Reich et al. 2007). However,

because plant and animal prey demand specificities in

their digestive process, this diet shift may have an impact

on green turtle digestive efficiency and, consequently, on

nutrient and energy assimilation (King 1996).

Some studies have shown that green turtles may

maintain a level of omnivory throughout ontogeny as

opposed to becoming obligate herbivores in the neritic

zone (e.g., Seminoff et al. 2002; Amorocho and Reina

2007; Carrion-Cortez et al. 2010). Despite the fact that the

consumption of animal matter by green turtles in South

Atlantic neritic habitats has already been reported (e.g.,

Ferreira 1968; Bugoni et al. 2003; Guebert-Bartholo et al.

2011; Reisser et al. 2013), including ingestion of large

amounts of animal matter (Gonzales Carman et al. 2014),

none of these authors discussed the possibility of an

ontogenetic dietary shift for green turtles in the South

Atlantic.

Additionally, the existence of a transitional stage

from carnivory to herbivory has been shown in the

Mediterranean Sea through stable isotopes (Cardona et al.

2010). In this study, Cardona et al. (2010) found that

seagrass prevailed in the stomach contents of all turtles,

but the concentration of stable isotopes in turtles shorter

than 40 cm of CCL suggested that just a negligible

amount of the nutrients assimilated were derived from

seagrass and that the contribution of seagrass nutrients

increased with turtle size. Their findings suggested that

turtles shift rapidly to an herbivore diet after the

recruitment to neritic habitats, although the green turtle

growth continues to rely on animal-derived nutrients for

several years. Although the stable isotopes analyses were

a powerful tool to estimate green turtles’ diet, a correct

interpretation of the results is not easy due to a number of

reasons such as: a large difference between the isotopic

signals of the diet items is required; an isotopic

characterization of various food sources is needed to gain

a better interpretation of the results; animals assimilate

dietary components with varying efficiencies; animal

tissues fractionate isotopes in their diet; and animals

allocate nutrients in their diet differentially to specific

tissues (Gannes et al. 1997; Cardona et al. 2010).

Therefore, the importance of conventional gut-content

analysis to improve the confidence of such estimates has

been highlighted in the literature (Hatase et al. 2006). So,

although the ontogenetic shift in diet is a widely accepted

phenomenon, much still remains to be understood about

it, especially due to the behavior plasticity found in some

areas (Hatase et al. 2006; Arthur et al. 2008). Here we

provide information on the diet of juvenile green turtles

from neritic developmental habitats of subtropical South

Atlantic that supports the existence of a gradual shift

from primarily carnivorous to a primarily herbivorous

diet.

Study Area. — The study was conducted at the

central and northern coasts of Santa Catarina State, south

Brazil, between the cities of Florianopolis (lat 27u369S,

long 48u339W) and Sao Francisco do Sul (lat 26u159S,

long 48u389W; Fig. 1) from 2006 to 2009. This region is

part of the Southern Brazilian shelf and is directly

influenced by the Subtropical Convergence, where the

cold-water, nutrient-rich Falklands current encounters the

warm-water, oligotrophic Brazilian current (Carvalho et

al. 1998). In the winter the feeding grounds are also

Figure 1. Map of the Santa Catarina State coast in southernBrazil. All stranded turtles were collected between Florianopolisand Sao Francisco do Sul.

NOTES AND FIELD REPORTS 261

heavily influenced by the Prata River (Pimenta et al.

2005). The rocky reefs, estuaries, bays, and coastal

ecosystems are important feeding grounds for immature

green sea turtles, C. mydas (e.g., Reisser et al. 2008, 2013;

Proietti et al. 2009; Guebert-Bartholo et al. 2011;

Gonzalez Carman et al. 2012).

Stranded Animals and Dietary Analysis. — Twenty-

six dead green turtles found stranded on the beach were

collected from 2006 to 2009; their CCL (± 0.1 cm) was

measured and stomach contents collected and preserved

in 4% formalin solution. Four individuals had empty

stomachs or a very small quantity of items (,± 5 g) and

were not considered in the analysis.

Dietary items were identified to the lowest taxonomic

level possible, and the frequency of occurrence, volume

(with precision of 0.5 ml; via water displacement), and

wet weight (with a precision of 0.0001 g) were quantified.

A minimum of 0.05 g was considered to define a

weighable item. All analyses were based on wet weight

due to its higher precision and high correlation with

volume (Spearman correlation, R 5 ± 0.99, p , ± 0.05).

We used Shapiro-Wilk tests to evaluate normality and

linear regression analysis to test the relationship between

CCL and the proportion of vegetal matter in the diet of

green turtles. We used analysis of similarity (ANOSIM) to

assess if individuals segregated according to stranding

season, stranding year, and trophic category. ANOSIM is a

multivariate permutation-based test which operates directly

in a dissimilarity matrix. The Bray-Curtis similarity matrix

was generated from the relative weigh of diet items

ingested by each turtle. Trophic categories were assigned to

each individual based on the proportion of vegetal matter

wet weight in the stomach content; primarily carnivorous

(less than 25%), omnivorous (25%–75%), and primarily

herbivorous (more than 75%).

Results. — All analyzed individuals were considered

juveniles, with CCL ranging from 23.5 cm to a maximum

of 50 cm (mean ± SD 5 35.84 ± 5.54 cm, n 5 22).

Total wet weight of stomach contents varied between 6.23

and 136.63 g (n 5 22), with an average of 43.17 g.

Neither season nor year of stranding significantly grouped

individuals (ANOSIM Season Global R 5 20.01,

p 5 0.50; Year Global R 5 0.13, p 5 0.10). They were,

however, grouped in trophic categories (ANOSIM Global

R 5 0.51, p , 0.01).

Algae (mainly Pterocladiella capillacea and Sargas-sum spp.), gelatinous animal matter from Cnidaria and

Ctenophora, and plant material consisting mainly of leaves

and stalks from Angiospermae were the most important

feeding items of the stranded turtles (Table 1). Other

animal items ingested included a small quantity of bivalve

and gastropod shells, urchin spines probably ingested

accidentally, and cephalopod beaks from pelagic deep sea

squids (more details in Morais et al. 2012). Anthropogenic

debris was present in 81% of the individuals and in some of

them composed more than 20% of the content weight.

Primarily herbivorous individuals (n 5 11) had algae

as their main feeding item (Table 1), especially P.capillacea, while primarily carnivorous individuals (n 5

8) relied on cnidarians and ctenophore gelatinous matter as

their most important feeding item. Omnivorous individuals

(n 5 3) had algae as their most important feeding item but

with animal matter showing considerable importance as

well (Table 1).

The linear regression highlights a significant posi-

tive relation between the proportion of vegetal matter

(angiosperms, algae, or both) ingested and the CCL

(R2 5 0.24, F 5 6.41, p 5 0.02, n 5 22, Fig. 2).

Discussion. — Larger juvenile green turtles tended to

ingest more vegetal matter than do smaller turtles,

Table 1. Relative weight (W%) and frequency of occurrence (FO%) of diet items found in stomach contents of stranded green turtleson the coast of Santa Catarina, south of Brazil. Primarily herbivorous (n 5 11), omnivorous (n 5 3), and primarily carnivorous(n 5 8).

W% (FO%)

Diet item Primarily herbivorous Omnivorous Primarily carnivorous

Algae 88.1 (100) 46.2 (100) 4.7 (87.5)Pterocladiela capillacea 47.5 (58.3) 5.4 (66.6) 0.0 (0.0)Sargassum spp. 7.6 (41.7) 40.6 (66.6) 3.8 (75.0)Codium spp. 5.3 (66.7) 0.0 (0.0) 0.0 (0.0)Gelidium floridanum 23.9 (8.3) 0.0 (0.0) 0.0 (0.0)Porphyra spp. 1.1 (25.0) 0.0 (0.0) 0.0 (0.0)Lobophora variegata 0.3 (8.3) 0.0 (0.0) 0.5 (12.5)Canistrocarpus cervicornis 0.5 (8.3) 0.0 (0.0) 0.0 (0.0)Hypnea musciformis 0.4 (8.3) 0.0 (0.0) 0.0 (0.0)Ulva spp. ,0.1 (8.3) 0.0 (0.0) 0.3 (12.5)Gelidiopsis gracilis 0.1 (8.3) 0.0 (0.0) 0.0 (0.0)Sphacelaria sp. 0.0 (0.0) 0.0 (0.0) 0.2 (12.5)Arthrocardia stephensoni 0.1 (8.3) 0.0 (0.0) 0.0 (0.0)Others 1.1 (16.7) 0.2 (33.3) 0.0 (0.0)

Animal 2.5 (36.4) 46.3 (100) 90.4 (100)Cnidaria + Ctenophora 2.5 (36.4) 46.3 (100) 90.4 (100)

Plant 9.4 (50.0) 7.2 (100) 4.9 (75.0)Terrestrial and marine

Angiospermae 9.5 (50.0) 7.2 (100) 4.9 (75.0)

262 CHELONIAN CONSERVATION AND BIOLOGY, Volume 13, Number 2 – 2014

suggesting the existence of a dietary shift from carnivory

to herbivory in coastal waters of the Southwestern

Atlantic. We believe that the existence of a neritic group

of individuals still relying on animal matter as an

important feeding source (primarily carnivorous and

omnivorous individuals) could corroborate the hypothesis

of a transitional stage between carnivory and herbivory in

recently recruited green turtles (Arthur et al. 2008;

Cardona et al. 2010). Although our sample size was

relatively small, we believe our results are representative

based on the following: 1) all individuals were fresh dead

and found stranded at the beach; therefore, these animals

might have already been recruited prior to death; 2) all

algae species found in the stomach contents are

commonly found in rocky reefs of the study area (Bouzon

et al. 2006; Horta et al. 2008), suggesting that those

individuals were foraging in the neritic zone; and 3)

stomach contents were collected throughout a relatively

long period (2006 to 2009), thus minimizing the influence

of a stochastic change in the availability of animal prey

in our results. Despite the presented reasons for the

representativeness of our sample, and the evident

influence of turtle size (CCL) on vegetal matter ingestion,

care must be taken in the interpretation of our results.

Small samples are more susceptible to individual

variations, and the stomach contents represent only a

snapshot of individual foraging pattern which provides

limited data to infer the long-term diet composition of

individuals. Therefore, our results may be explained by

other reasons, such as individual specializations, as found

in other studies (e.g., Burkholder et al. 2011).

The importance of algae for adult green turtles’ diet

has been observed worldwide (Bjorndal 1997). Thepresent study shows that most of the stranded juvenileC. mydas also relied on algae as their main food source.Regardless of the number of different taxa found, P.capillacea (for the primarily herbivorous individuals) and

Sargassum spp. (for the omnivorous individuals) were theonly species considerably important in the diet of theseanimals. A similar result was found in a study conductedin the same region (Reisser et al. 2013). Besides, thesespecies are relatively common in the diet of green turtlesfrom other places (Balazs 1980; Sazima and Sazima 1983;Lopez-Mendilaharsu et al. 2005; Russel and Balazs 2009).The high relative importance of Sargassum spp. for theomnivorous turtles is unexpected because previous studies(e.g., Seminoff et al. 2002) suggested that green turtleshave difficulty in digesting this genus. This Sargassum spp.ingestion is probably related to the green turtle pelagicforaging strategy utilized to feed on ctenophores. BecauseSargassum spp. have air bladders (floating structure),which provide positive buoyancy, omnivorous turtlesduring their water column foraging will have higherchances of encountering Sargassum spp. than other benthicalgae species. The relation between pelagic foragingstrategy and Sargassum spp. ingestion was found in otherareas along the Brazilian coast (R.G. Santos, unpubl. data,2014).

Herbivory represents a challenge for marine reptiles

in terms of energy and digestibility (Bjorndal 1995;

King 1996). Several aspects are related to the diges-

tive efficiency in C. mydas such as water temperature,

individual size, and intestinal microbiota (Bjorndal 1980).

The green turtle is an ectothermic species which at best

maintains a temperature 1u–2.5uC above environmental

temperature when inactive (Heath and McGinnis 1980;

Standora et al. 1982); however, green turtles can maintain

higher body temperatures during vigorous activities

(Standora et al. 1982). The capacity to maintain more

constant and relatively high body temperatures is

influenced by the size of the turtle, where larger

turtles are able to maintain constant and relatively high

temperature more easily than do smaller turtles because of

their smaller surface area to volume ratio (Spotila et al.

1991). Thus, low water temperatures will have a stronger

effect in the digestive efficiency of small turtles than in

large turtles. In the South Brazilian shelf, the mean

shallow-water temperature ranges from 24u–25uC in the

summer and from 17u–18uC in the winter (Carvalho et al.

1998), but temperatures as low as 13uC are sometimes

observed in the study area. Therefore, the water temper-

ature in our study area may have a stronger negative effect

in the digestibility efficiency of the smaller turtles, thus

favoring the ingestion of animal matter (ctenophores),

which may be easier to digest than vegetal matter due to the

relatively low fiber content and the absence of cell walls.

Additionally, measurements of rate of digestion in fishes

showed that ctenophores are digested 20 times faster than

other invertebrates (Arai et al. 2003).

Another important aspect of the digestion of vegetal

matter in many herbivorous taxa is the presence of a

specialized gut microbiota (Horn 1989; King 1996; Choat

and Clements 1998). In green turtles, diet-optimized gut

microbial communities are recognized as components of

their optimal foraging strategy (Bjorndal 1980). However,

Figure 2. Linear regression between the proportion of vegetalmatter in the stomach contents and size (curved carapace length;CCL) of stranded green turtles in Santa Catarina, south of Brazil.The trophic categories were assigned based on the proportionof vegetal matter wet weight in each individual’s stomach;primarily carnivorous (less than 25%), omnivorous (25%–75%),and primarily herbivorous (more than 75%).

NOTES AND FIELD REPORTS 263

when or how this specific microbiota is acquired remains

unknown. Therefore, green turtles recently recruited to

neritic habitats may have not yet acquired the gut

microbiota needed to efficiently digest vegetal matter;

this may favor a diet based on items with a relatively easy

digestion such as animal matter.

In parallel to that, small green turtles often have faster

growth rates and absorb a smaller percentage of nutrients

than do larger ones (Bjorndal et al. 2000). This could mean

that small individuals need to consume proportionally more

energy than do large individuals, either through the

ingestion of proportionally more food or through the

ingestion of higher-quality food. Animal tissues are

considered to be a high-quality source of food in

comparison with plant material because they present higher

energetic and nutrient content (Newman 2007). The

increase of digestive efficiency with size may be due 2

main factors: the increase of thermal inertia due to the

larger body size, which is beneficial for maintain an active

gut microbiota (Bjorndal 1985); and the increase of

intestinal volume which, besides increasing the food

passage time, provides a better environment for food

fermentation (Bjorndal and Bolten, 1990; King 1996).

Therefore, 3 hypotheses could account for the lower

ingestion of vegetal matter by smaller individuals: 1)

smaller turtles ingest relatively more digestible items

(e.g., ctenophores) rather than vegetal matter due to the

reduction of the digestion efficiency imposed by the low

water temperature; 2) smaller individuals recently recruit-

ed to the neritic zone may not have acquired a well-

adapted gut microbiota for digestion of vegetal matter; as

a result they are more prone to feeding on animal matter

than are older individuals; and 3) smaller individuals, with

higher growth rates, ingest preferentially high-quality

food despite the abundance of low-quality food on the

hard substrate of coastal habitats. It is important to note

that these hypotheses are not mutually exclusive but

rather could act simultaneously to generate the observed

pattern. Although these hypotheses can explain our

results, they need to be adequately tested by means of

choice experiments and investigation of gut microbiota in

individuals of a wide range of sizes.

We believe that the combination of the low water

temperature, green turtles’ size, and microbiota acquisi-

tion may favor the occurrence of a transitional stage from

primarily carnivorous to primarily herbivorous in our

study area. To our knowledge, this is the first report of the

evidence of a transitional stage in the South Atlantic,

although many diet studies have been conducted in this

area (e.g., Ferreira 1968; Sazima and Sazima 1983;

Bugoni et al. 2003; Guebert-Bartholo et al. 2011;

Nagaoka et al. 2011; Santos et al. 2011). Most of these

studies were conducted in warmer areas or with larger

animals (or both), which may explain that a transitional

stage has never been reported before. The existence of

this transitional period may not be mandatory to green

turtles but may arise from specific conditions such as

seasonal abundance of macrozooplankton (Gonzalez

Carman et al. 2012) and low water temperatures.

Understanding the foraging strategy helps to clarify

how the species maximizes its fitness in a particular

habitat. Information regarding foraging is crucial not

only for ecological knowledge of a species but also for

helping us to anticipate potential threats in particular

habitats.

Acknowledgments. — Projeto Tamar, a conservation

program of the Brazilian Ministry of the Environment

(MMA), is affiliated with the Chico Mendes Institute for

Biodiversity Conservation (ICMBio/MMA), is coman-

aged by Fundacao Pro-Tamar, and is officially sponsored

by Petrobras. R.A. Morais and G.O. Longo were granted

scholarships from CAPES, Brazilian Ministry Educational

Council. P.A. Horta was granted a fellowship from CNPq

and funding from CNPq and CAPES.

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NOTES AND FIELD REPORTS 265

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Received: 2 May 2013

Revised and Accepted: 8 May 2014

Handling Editor: Jeffrey A. Seminoff

266 CHELONIAN CONSERVATION AND BIOLOGY, Volume 13, Number 2 – 2014