· the present study analysed ontogenetic diet changes and food partitioning in haemulon spp. we...

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Reviews in Fish Biology and Fisheries ISSN 0960-3166 Rev Fish Biol FisheriesDOI 10.1007/s11160-014-9378-2

Ontogenetic diet changes and foodpartitioning of Haemulon spp. coral reeffishes, with a review of the genus diet

Pedro Henrique Cipresso Pereira,Breno Barros, Rahel Zemoi & BeatricePadovani Ferreira

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RESEARCH PAPER

Ontogenetic diet changes and food partitioning of Haemulonspp. coral reef fishes, with a review of the genus diet

Pedro Henrique Cipresso Pereira •

Breno Barros • Rahel Zemoi •

Beatrice Padovani Ferreira

Received: 2 April 2014 / Accepted: 4 November 2014

� Springer International Publishing Switzerland 2014

Abstract The genus Haemulon contains some of the

most abundant and ecologically important reef fishes

in the South Atlantic Ocean. However, their life

history attributes have not been widely studied.

Knowledge of ontogenetic changes in their resource

use is critical to understanding the processes structur-

ing natural communities. The present study analysed

ontogenetic diet changes and food partitioning in

Haemulon spp. We collected stomach contents from

276 individuals of four different size classes from four

sympatric species (H. aurolineatum, H. parra, H.

plumieri and H. squamipinna). There was a significant

difference in the proportions of prey types between

both species and size classes, providing evidence of

food partitioning. Moreover, the Bray–Curtis similar-

ity index revealed two distinct groups. The first

consisted of larger-sized fish that consumed larger

food items and the second group consisted of smaller

individuals that fed on small invertebrates. There was

an abrupt shift in the diet of Haemulon spp. at around

10.0 cm total length, a size that corresponds with the

greatest morphological changes in the genus. Addi-

tionally, the diet overlap calculated by Pianka’s index

was more evident in smaller and larger size classes

than in intermediate individuals. Together, these

observations suggest Haemulon species undergo onto-

genetic diet changes and food partitioning within

species and size classes that are associated with

changes in their habitat use, alongside morphological

changes. Further research is needed to determine their

ecomorphology and the competitive mechanisms that

allow the coexistence of several sympatric and eco-

logically similar species of the genus Haemulon.

Keywords Diet composition � Resources partition �Haemulidae � Northeast Brazil

Introduction

Coral reefs are productive habitats that offer shelter to

a highly diverse predator and prey fauna within a

complex suite of trophic relationships (Connell 1978;

Edgar and Shaw 1995). For example, the substratum

can provide habitat for many invertebrates, such as

crabs and polychaetes, which in turn represent a food

resource for several reef fishes (Parrish et al. 1985).

Coral reef fishes are one of the most diverse taxa on

coral reefs and are represented in all the trophic guilds

P. H. C. Pereira (&) � R. Zemoi

School of Marine and Tropical Biology, James Cook

University (JCU), Townsville, QLD 4811, Australia

e-mail: [email protected]

P. H. C. Pereira � B. P. Ferreira

Departamento de Oceanografia, CTG, Universidade

Federal de Pernambuco (UFPE), Av. Arquitetura, s/n,

Cidade Universitaria, Recife, PE 50670-901, Brazil

B. Barros

Museu Paraense Emılio Goeldi, Av. Perimetral SN,

Belem, Para CEP 66077-830, Brazil

123

Rev Fish Biol Fisheries

DOI 10.1007/s11160-014-9378-2

Author's personal copy

(Ferreira et al. 2004). Consequently, species diet

plasticity and ontogenetic shifts must be taken into

account during classification of reef fish into trophic

groups (Jones et al. 1991; Ferreira et al. 2004).

A large number of reef fish exhibit ontogenetic diet

changes (Schmitt and Holbrook 1984; Winemiller

1989; McCormick 1998; Grutter 2000; Dahlgren and

Eggleston 2000; Figueiredo et al. 2005). The size of

food items that are consumed is one of the most

important factors correlated with these changes (Lu-

koschek and McCormick 2001). Furthermore, changes

in species habitat use, anatomical and morphological

variation, behaviour, and feeding rates are also

important when considering ontogenetic diet changes

in reef fishes (Schmitt and Holbrook 1984; Lukoschek

and McCormick 2001; Barros et al. 2011; Pereira and

Ferreira 2013). Generally, juvenile reef fish are more

active and have higher feeding rates compared with

adults that consume larger prey (Blueweiss et al. 1978;

Yager and Summerfelt 1993). Therefore, shifts in

resource associated with ontogeny normally minimize

energetic cost and predation risk while maximizing

growth rates (Grossman 1980; Brown et al. 2002).

Differences in resource use between competing

species provide a mechanism of sustaining diverse

fauna in complex ecosystems (Pianka 1970; Colwell

and Fuentes 1975). Resource partitioning theory

predicts that whenever a species decreases the use of

shared available resources by specializing on a

specific resource, conspecific competition will

decrease more rapidly than intraspecific competition

will increase (Colwell and Fuentes 1975). Niche

partitioning can occur in three basic ways (Amarasek-

are 2003). First, the classic resource partitioning

theory assumes that different species may specialize

on distinct resources (MacArthur and Levins 1967).

Second, temporal niche partitioning predicts that

different species may be limited by the same

resources, but differ in terms of when they exploit

the resource (Armstrong and McGehee 1980; Chesson

1985). Third, species could differ in terms of where

they use their resources, thereby exhibiting spatial

niche partitioning (May and Hassell 1981; Chesson

2000). Food partitioning in regard to time and space

seems to play an important role in reef fish coexistence

(Armstrong and McGehee 1980; Pimentel and Joyeux

2010; Wollrab et al. 2013) by reducing competition

levels on sympatric species (Nithirojpakdee et al.

2012).

Species of the genus Haemulon (commonly known as

grunts) are known to conduct daily migrations from the

reef to the soft bottom, macroalgae, and seagrass beds in

tropical areas of the Caribbean and NE Brazil. These

migrations are correlated with ontogenetic changes in

their diet (Parrish 1989; Cocheret de la Moriniere et al.

2003; Nagelkerken et al. 2000; Pereira et al. 2010).

Furthermore, the feeding behaviour and the proportion of

food items consumed by grunts changes significantly

during ontogeny (Nagelkerken et al. 2000; Cocheret de la

Moriniere et al. 2003; Pereira and Ferreira 2013).

Juveniles feed primarily on small planktonic invertebrates

(e.g., copepods, amphipods, crustaceans, and polychae-

tes). In contrast, adults tend to feed exclusively on the

benthos, eating more brachyuran crabs and polychaetes

(Cocheret de la Moriniere et al. 2003). Individuals of the

genus Haemulon are also known to display changes in

foraging behaviour according to life phase and schooling

patterns. Juveniles tend to feed in the water column,

whereas adults forage primarily on sand and rock (Pereira

and Ferreira 2013). Despite this knowledge, changes in

the diet composition according to ontogeny and food

partitioning have never been analysed for Haemulon

species in the South Atlantic Ocean where they have

ecological, economical, and social importance on tropical

coral reefs (Rocha et al. 2008; Pereira et al. 2011, 2012;

Pereira and Ferreira 2012).

The present study aimed to analyse ontogenetic diet

changes and food partitioning of four competing

sympatric species of the genus Haemulon (H. auroline-

atum, H. parra, H. plumieri and H. squamipinna).

According to previous research, the four species have

similar habitat use, behaviour, and distribution in the

Atlantic Ocean (Rocha et al. 2008; Pereira and Ferreira

2013). Therefore, we tested the following questions: (1)

is there an ontogenetic diet shift within Haemulon

species and across different size classes (\5, 5.0–10,

10.0–15.0, and [15 cm)? and (2) is there any food

partitioning or diet overlap across species and size

classes? Additionally, we included a complete review on

the genus diet, including life phase and habitat use data.

Materials and methods

Study area

The studied reef complex is within the limits of the

‘‘Costa dos Corais’’ Marine Protected Area (MPA)


123


that encompasses 135 km of coastline in Pernambuco

State of Northeastern Brazil. The ‘‘Costa dos Corais’’

MPA was the first Brazilian federal conservation area

that included coastal reefs and is the largest multiple-

use MPA in the country, encompassing an area of

413,563 ha (Maida and Ferreira 1997). The area has a

tropical climate with an intercalary regime of wet

(October–May) and dry (May–September) seasons

with maximum temperatures of 26–30 �C (Maida and

Ferreira 1997). The tropical coral reef ecosystem in

the Pernambuco State municipality of Tamandare is

composed of three main reef lines parallel to the coast

(Fig. 1). This research was carried out specifically on

the two most inshore reefs, as the most offshore reefs

are deeper and not yet well surveyed. The first reef is

typically exposed during the largest tidal amplitudes

and consists of large algae beds composed primarily of

macroalgae of the genera Sargassum, Caulerpa,

Udotea, Neomeris, Padina, Gracilaria, Dictyota and

encrusting coralline algae Halimeda opuntia. The

second reef is more diverse in terms of habitat,

comprising small patch reefs, narrow channels, and

pools with sandy bottoms. This habitat remains mostly

submerged during low tide. The last reef represents the

characteristic shape of Brazilian coral reefs, which is

distinct from other reef systems, developing in isolated

columns of 1.2–2.0 m that coalesce at the top (Maida

and Ferreira 1997).

Collection of individuals and stomach analyses

Haemulon spp. individuals were collected multiple

times across 1 year (from December 2009 to Decem-

ber 2010) using different fishing gears to encompass

all the size classes (hand net, hook-and-line and spear

fishing). Sampling was performed along the coastal

reefs of Tamandare municipality, NE Brazil (Fig. 1).

Because Haemulon species migrate from reef to soft

bottoms at night (Cocheret de la Moriniere et al. 2002;

Burke et al. 2009), their diet may differ between day

and night. If individuals were not collected consis-

tently in the middle of the day and/or afternoon, items

ingested during the previous night would be digested

and impossible to identify. Therefore, all the samples

were collected in the middle of the day and afternoon

to avoid this issue.

After collection, all individuals were weighed, their

total length (TL) measured and the stomach contents

removed and preserved in 70 % ethanol. To analyse

ontogenetic diet changes, species were assigned into

four different size classes: Class 1 (\5.0 cm), Class 2

(5.0–10.0 cm), Class 3 (10.0–15.0 cm), and Class 4

Fig. 1 Study area highlighting the coral reef ecosystem of Tamandare complex, NE Brazil, where Haemulon spp. individuals were

collected


123


([15.0 cm). Individuals of the genus Haemulon also

exhibit ontogenetic patterns of coloration; therefore

these patterns were used to identify species and life

phases (Fig. 2).

Using a stereomicroscope, the relative volumetric

amount of the food items was estimated, i.e., the

volume of the contents of the digestive tract was set to

100 %, and the volumetric percentage of each food

item relative to the total stomach volume was

estimated by eye (Nielsen and Johnson 1992). A

volumetric measure was chosen because it is an

estimation of biomass, whereas gravimetric methods

would produce large errors with small volumes

because of water content (blotting would damage the

samples in some cases). Additionally, methods that

involve frequencies would underestimate large food

items and overestimate small food categories (Hyslop

1980).

Food components in the digestive tracts were

classified as Bivalvia, Gastropoda, Polyplacofora,

Cumacea, Nematoda, Ostracoda, Polychaeta, Tanaid-

acea, Copepoda, Isopoda, Amphipoda, Caridae, Sto-

matopoda, Brachyura, unidentified crustaceans, fish

fragments (e.g., scales and spines), sand or algae.

Fig. 2 Ontogenetic patterns of coloration displayed by indi-

viduals of the genus Haemulon and used to identify species and

life phases. a H. aurolineatum juvenile, b H. aurolineatum adult,

c H. parra juvenile, d H. parra adult, e H. plumieri juvenile, f H.

plumieri adult, g H. squamipinna juvenile, h H. squamipinna

adult


123


Statistical analyses

We tested for differences in the stomach contents

using a two factor permutational multivariate analysis

of variance (PERMANOVA). Factor 1 comprised fish

‘Species’, with four categories (H. aurolineatum. H.

parra, H. plumieri and H. Squamipinna). Factor 2,

included ‘Size Classes’, also with four categories—

Class 1 (\5.0 cm), Class 2 (5.0–10.0 cm), Class 3

(10.0–15.0 cm) and Class 4 ([15.0 cm). During the

test, species and size classes were fixed factors,

whereas the percent volume of each food item (log

transformed) was a dependent variable. All factors

were independent and not random. This method

analyses the variance of multivariate data explained

by a set of explanatory factors based on any distance or

dissimilarity measure of choice. The method provides

P values by permutations, so that effects linked to each

factor or interaction between factors may be tested in a

robust way (Anderson et al. 2008).

The degree of food overlap among species and size

classes was analysed using a food overlap index

developed by Pianka (1973):

Oxy ¼ Oyx ¼ R XiYi=p

RXi2 � RYi2

where Oxy and Oyx represent the food overlap

between species X and Y, while Xi and Yi represent

the food item proportions. The results from the Pianka

(1973) index vary from 0 to 1, with 0 representing

complete food partitioning and 1 a total food overlap.

Moreover, values greater than 0.60 represent a high

degree of diet overlap among species and size classes

(Zaret and Rand 1971).

Multivariate analyses were also performed in

regard to the diet and size classes in the genus

Haemulon: (1) Multidimensional scaling (MDS) was

used to evaluate the proportion of the four most

important food items in regard to size (copepoda,

amphipoda, polychaetes and brachyura). (2) Cluster

analysis using the Bray–Curtis similarity index was

used to group size classes in relation to stomach

contents, and (3) Principal component analysis

(PCA) by species and size classes was used to

show the relationship between Haemulon spp. and

their diet. All the data were standardized and log-

transformed before multivariate analyses were

performed.

Primer-e 6 PERMANOVA?1.0 software (Ander-

son et al. 2008) was used to conduct the PERMANO-

VA and multivariate analyses.

Results

The proportion of prey types in the diet differed

between fish size classes for all the analysed species

(Table 1). Among the small size class (\5.0 cm), we

observed a high percentage of copepoda (34 % of the

total stomach volume) and amphipoda (20 %) in the

diet, with some differences between species. For

example, almost 25 % of the stomach contents of H.

aurolineatum was unidentified crustaceans. In con-

trast, for larger size individuals ([15.0 cm) polychae-

tes represented the most important food item (around

40 % of the stomach volume), followed by fish

fragments (e.g., scales and spines) which accounted

[15 % of the volume (Table 1). Overall, all four

Haemulon species were classified as mobile inverte-

brate feeders, capturing prey on the bottom or in the

water column depending on their size, and having a

variety of crustaceans and polychaetes in their stom-

achs (Table 1). Nevertheless, prey items of different

sizes (up to 100-fold difference) were observed in the

Haemulon spp. stomachs (Fig. 3).

PERMANOVA analyses revealed a significant

difference in the percent volume of food items between

both species (PERMANOVA, F = 7.874, P \ 0.001)

and size classes (PERMANOVA, F = 17.252,

P \ 0.001) (Table 2). Although the main food items

were similar, Haemulon species used different pro-

portions of prey between each size class (Tables 1, 2).

The four most common food items (copepoda,

amphipoda, polychaetes and brachyura) and their

proportional abundance for each size classes are

illustrated by MDS (Fig. 4). Copepoda were the most

common food item in the stomachs of H. parra, H.

aurolineatum, and H. squamipinna smaller than

5.0 cm, followed by amphipoda in individuals up to

10.0 cm. In contrast, polychaetes and brachyura were

very abundant in all Haemulon species [10.0 cm

(Fig. 4).

The dendrogram generated from the Bray–Curtis

similarity index using percentage of food items

revealed two distinct groups, with 45 % of similarity


123


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123


(Fig. 5). The first group consisted of larger size classes

that consumed mostly large items (e.g., polychaetes,

brachyura, and fish fragments). The second group

consisted of smaller individuals (\10.0 cm) that fed

preferentially on tanaidacea, copepoda, ostracoda,

isopoda, and amphipoda.

The PCA performed explained 64.4 % of the total

variability in food items, with 47.5 % of the variability

explained by PC1 (Eigenvalue 718) and 16.9 % by

PC2 (Eigenvalue 256) (Fig. 6). This analysis suggests

that small (\5.0 cm) and medium size classes

(5.0–10.0 cm) fed more on small invertebrates such

as copepoda, tanaidacea, amphipoda, and ostracoda.

In contrast, larger individuals had a higher proportion

of polychaete, brachyura, and fish fragments in their

stomachs (Fig. 6).

Diet overlap was estimated using Pianka’s index

and suggested that the food overlap for grunts species

was more evident in smaller and larger size classes,

compared with intermediate individuals (Table 3). For

instance, the diet overlap of individuals from 0 to 5 cm

between H. aurolineatum and H. squamipinna was

0.90. Similarly, the diet overlap between H. auroline-

atum and H. plumieri larger than 15 cm was high

(0.97). In contrast, for intermediate sized individuals

such as H. aurolineatum and H. squamipinna ranging

from 10 to 15 cm, diet overlap values were low (0.38)

(Table 3).

The most comprehensive review to date of the

genus Haemulon diet was also performed during the

Fig. 3 Food items recorded in Haemulon spp. stomachs, demonstrating the difference in size of items consumed (up to 100 9 mm)

Table 2 PERMANOVA analyses of the diet (% volume) of

four Haemulon species (H. aurolineatum, H. parra, H. plumieri

and H. squamipinna) and size classes (\5, 5.0–10, 10.0–15.0

and [15 cm)

Source df SS MS F P

Species 3 6.0805 20,268 7.8746 \0.001

Size classes 3 1.3324 44,414 17.256 \0.001

Esp. 9 size clas. 9 1.1464 12,738 4.9489 \0.001

Res 224 5.7655 2,573.9 – –

Total 239 8.8524 – – –


123


Fig. 4 nMDS for the most common food items. a Copopoda, b Amphipoda, c Polychaeta, d Brachyura. The circles represent the

percent of the food item in the stomachs of different size classes of Haemulon spp.

Fig. 5 Similarity analyses using Bray–Curtis index with data clustered by percent of food items for Haemulon species and size classes.

H. aur, Haemulon aurolineatum; H. squ, Haemulon squamipinna; H. par, Haemulon parra; H. plu, Haemulon plumieri


123


present study (Table 4). In this review, 13 Haemulon

spp. were analysed by life phase, habitat use, food

habits (% volume), and location. A total of five studies

that were distributed across the Atlantic Ocean were

included in the review (Table 4).

Discussion

The four grunt species analyzed during the present

study exhibited ontogenetic diet changes within a

South Atlantic coral reef complex. Changes in habitat

use, morphology, and anatomy are important explan-

atory variables of diet shifts in coral reef fishes

(Schmitt and Holbrook 1984; McCormick 1998;

Dahlgren and Eggleston 2000). Based on the food

items observed in the stomach contents, it is clear that

the diet of these four grunts change as a result of

changes in feeding behaviour and the preferred

feeding habitat (e.g., water column or benthic sub-

stratum). According to Pereira and Ferreira (2013),

species of the genus Haemulon have similar patterns

of feeding behaviour. However, their feeding habitat

and foraging rates change considerably during their

life history. Juveniles have high feeding rates in the

water column, whereas adults have low feeding

frequency and forage the benthic substratum (Pereira

and Ferreira 2013). This is consistent with our analysis

of stomach contents, which suggested that copepods

(planktonic species) and amphipods dominate the

stomach contents of small Haemulon spp. individuals;

whereas benthonic crabs and polychaetes were the

dominant prey items of adults.

Cocheret de la Moriniere et al. (2003) analysed

ontogenetic changes in grunt diet in the Caribbean and

also documented a change in the type of food items

consumed associated with growth. Small body size

(B5.0 cm) H. flavolineatum individuals fed primarily

on copepods (80.0 % of the stomach content). In

contrast, larger H. flavolineatum individuals

(C10.0 cm) consumed a higher proportion of mid-

sized crustaceans, such as tanaidacea (up to 50.0 % of

Fig. 6 PCA for the most important food items and size classes of the four Haemulon species


123


the stomach content). Additionally, decapoda repre-

sented approximately 70 % of the diet of larger H.

sciurus (C20.0 cm) (Cocheret de la Moriniere et al.

2003). Small food items such as copepods and

ostracods are common in the diets of post-settlement

coral reef fish, when individuals are observed feeding

in the water column (Austin and Austin 1971; Grutter

2000; Lukoschek and McCormick 2001). The use of

small crustaceans by juveniles of Haemulon species

can be correlated with their patterns of foraging

behaviour. Pereira and Ferreira (2013) observed a high

proportion of juveniles of the same grunt species

foraging in the water column. Moreover, juveniles of

multiple coral reef fish families have higher foraging

rates than do adults (Van Rooij et al. 1996; Nanami

and Yamada 2008). Feeding on more abundant

planktonic prey provides sufficient food resources to

sustain higher growth rates during the juvenile life

phase (Hernaman et al. 2009).

The most distinct ontogenetic diet shift was

observed for Haemulon spp. individuals of approxi-

mately 10 cm TL, with the cluster analysis revealing

two distinct groups. This is consistent with the

observations of Gaut and Munro (1983) and Lindeman

(1986) who concluded that the strongest morpholog-

ical and morphometric changes in Haemulon individ-

uals occurs at around 10.0 cm TL (ranging from 3.9 to

9.2 cm depending on the species). These morpholog-

ical and morphometric changes are correlated with

body shape, head size, and body pigmentation. For

example, Lindeman (1986) noted that the appearance

and subsequent loss of early juvenile pigmentation in

some Haemulon spp. often coincides with ontogenetic

shifts in habitat use and feeding strategies. This

indicates that those changes are strongly correlated

with ontogenetic migrations and camouflage, as

observed for other reef fishes (Feitosa et al. 2012).

Furthermore, grunts are known to perform ontogenetic

migrations that encompass coral reefs, mangroves, and

seagrass beds (Lindeman et al. 2000; Cocheret de la

Moriniere et al. 2002; Burke et al. 2009). These

migrations are associated with changes in photic

sensitivity, gonadal development, and swimming

performance (McFarland et al. 1979; Helfamn et al.

1982; Gaut and Munro 1983). In this context, changes

in habitat use can also induce significant ontogenetic

diet changes in grunts. Changes in habitat use affect

Haemulon spp. diet in several ways: (1) differences in

prey availability between coral reefs, mangroves, and

seagrass beds (Nakamura and Sano 2005; Casares and

Creed 2008) will result in changes in the diet of a

migratory individual; and (2) changes in the fish

community between mangroves and coral reefs (Oso-

rio et al. 2011; Xavier et al. 2012; Pereira et al. in

prep.) have a direct effect of competition processes

and thus influence the grunt’s diet, regardless of their

natural preference.

Crustaceans were the dominant food items in the

stomach of Haemulon spp. for all size classes, as in

several other reef fish (Lukoschek and McCormick

2001). Small crustaceans such as amphipoda, tanaid-

acea, and isopoda were the most important food items

for intermediate size classes (5.0–10.0 cm) during the

Table 3 Diet overlap of Haemulon spp. individuals collected

from Tamandare coastal reefs using Pianka index (1973)

Size Classes Diet overlap

Individuals from 0 to 5 cm –

H. aurolineatum 9 H. parra 0.809

H. aurolineatum 9 H. plumieri –

H. aurolineatum 9 H. squamipinna 0.904

H. parra 9 H. plumieri –

H. parra 9 H. squamipinna 0.758

H. plumieri 9 H. squamipinna –



H. aurolineatum 9 H. plumieri 0.664


H. parra 9 H. plumieri 0.819


H. plumieri 9 H. squamipinna 0.835








Individuals >15 cm –







Figures higher than 0.60 (bold) represent high diet overlap


123


Ta

ble

4R

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wo

fg

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sH

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wit

hd

ata

org

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edb

yli

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has

e,h

abit

atan

dsi

te

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ecie

sL

ife

ph

ase

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itat

Die

t—m

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rele

van

t

item

s(%

vo

lum

e)

Sit

eR

efer

ence

s

Ha

emu

lon

alb

um

Ad

ult

Co

ral

reef

sS

ipu

ncu

lid

s—2

5.2

/Ech

ino

ids—

19

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tlan

tic—

Car

ibb

ean

—W

est

Ind

ies

Ran

dal

l(1

96

7)

Ha

emu

lon

au

roli

nea

tum

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enil

eC

ora

lre

efs

Co

pep

od

a—3

7.3

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ph

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da—

27

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tlan

tic—

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rese

nt

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dy

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enil

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a—4

0.1

/Cla

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0.5

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anti

c—C

olo

mb

ia(S

anta

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ta)

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rad

a(1

98

6)

Ad

ult

Co

ral

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ni

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ean

s—3

4.2

8/P

oly

chae

tes—

31

.3A

tlan

tic—

Bra

zili

anC

oas

tP

rese

nt

stu

dy

Ad

ult

Co

ral

reef

sS

hri

mp

s—3

3.6

/Po

lych

aete

s—3

1.0

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anti

c—C

arib

bea

n—

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die

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and

all

(19

67

)

Ad

ult

Co

ral

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sG

astr

op

od

s—2

5.5

/Dec

apo

da—

15

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tic—

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ibb

ean

—W

est

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ies

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rad

a(1

98

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Ha

emu

lon

carb

on

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um

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ult

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ral

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s—3

8.3

/Gas

tro

po

ds—

15

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tlan

tic—

Car

ibb

ean

—W

est

Ind

ies

Ran

dal

l(1

96

7)

Ad

ult

Co

ral

reef

sA

mp

hip

od

a—2

0.5

/Gas

tro

po

ds—

15

.2A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)

Ha

emu

lon

chry

sarg

yreu

mJu

ven

ile

Co

ral

reef

sC

op

epo

da—

20

.3/C

rust

acea

nL

arv

ae1

0.5

Atl

anti

c—C

olo

mb

ia(S

anta

Mar

ta)

Est

rad

a(1

98

6)

Ad

ult

Co

ral

reef

sD

ecap

od

a—4

5.6

/Gas

tro

po

ds—

15

.5A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)

Ad

ult

Co

ral

reef

sD

ecap

od

a—1

9.4

/Po

lych

aete

s—1

9.1

Atl

anti

c—C

arib

bea

n—

Wes

tIn

die

sR

and

all

(19

67

)

Ad

ult

Co

ral

reef

sC

rust

acea

ns—

29

.0/P

oly

chae

tes—

18

.0A

tlan

tic—

Bra

zili

anO

cean

icIs

lan

dK

raje

wsk

i(2

01

0)

Ha

emu

lon

fla

voli

nea

tum

Juv

enil

eM

ang

rov

e/se

agra

ssC

op

epo

da—

37

.6/T

anai

dac

ea—

34

.1A

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tic—

Car

ibb

ean

—C

ura

cao

Co

cher

etd

ela

Mo

rin

iere

etal

.(2

00

3)

Juv

enil

eC

ora

lre

efs

Gas

tro

po

ds—

27

.6/C

op

epo

da—

24

.1A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)

Ad

ult

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ral

reef

sD

ecap

od

a—2

9.4

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lych

aete

s—2

1.1

Atl

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c—C

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mb

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ta)

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rad

a(1

98

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ve/

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rass

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tes—

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n—

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(19

67

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du

ltC

ora

lre

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ino

ids—

86

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l(1

96

7)

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ult

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ral

reef

sD

ecap

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a—2

7.9

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ea—

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(San

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stra

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(19

86

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0A

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stra

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(19

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ora

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pep

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a—3

5.1

/Tan

aid

acea

—2

4.1

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anti

c—B

razi

lian

Co

ast

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sen

tst

ud

y

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ult

Co

ral

reef

sP

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chae

tes—

61

.2/U

ni

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stac

ean

s—1

4.1

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anti

c—B

razi

lian

Co

ast

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sen

tst

ud

y

Ad

ult

Co

ral

reef

sS

hri

mp

s—3

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/Dec

apo

da—

33

.3A

tlan

tic—

Car

ibb

ean

—W

est

Ind

ies

Ran

dal

l(1

96

7)

Ad

ult

Co

ral

reef

sP

oly

chae

tes—

30

.0/C

rust

acea

ns—

13

.0A

tlan

tic—

Bra

zili

anO

cean

icIs

lan

dK

raje

wsk

i(2

01

0)

Ha

emu

lon

plu

mie

riJu

ven

ile

Co

ral

reef

sA

mp

hip

od

a—2

9.3

/Un

iC

rust

acea

ns—

23

.1A

tlan

tic—

Bra

zili

anC

oas

tP

rese

nt

stu

dy

Ad

ult

Co

ral

reef

sP

oly

chae

tes—

24

.5/B

raq

uiu

ra—

18

.4A

tlan

tic—

Bra

zili

anC

oas

tP

rese

nt

stu

dy

Ad

ult

Co

ral

reef

sB

raq

uiu

ra—

26

.0/P

oly

chae

tes—

14

.5A

tlan

tic—

Car

ibb

ean

—W

est

Ind

ies

Ran

dal

l(1

96

7)

Ha

emu

lon

sciu

rus

Juv

enil

eM

ang

rov

e/se

agra

ssC

op

epo

da—

37

.6/T

anai

dac

ea—

34

.1A

tlan

tic—

Car

ibb

ean

—C

ura

cao

Co

cher

etd

ela

Mo

rin

iere

etal

.(2

00

3)

Ad

ult

Man

gro

ve/

seag

rass

Dec

apo

da—

50

.2/U

nid

enti

fied

—1

5.2

Atl

anti

c—C

arib

bea

n—

Cu

raca

oC

och

eret

de

la

Mo

rin

iere

etal

.(2

00

3)


123


present study. These crustacean groups typically have

low dispersal capacity (Thomas 1993) and are pri-

marily associated with macroalgal beds (Jacobucci

and Leite 2002; Tanaka and Leite 2003) where they

are most likely preyed upon by the grunts. The

presence of algal fragments in the grunt’s stomachs is

indicative of incidental consumption of macroalgae

while feeding on associated invertebrates (Kotrschal

and Thomson 1986; Pereira and Jacobucci 2008;

Hammerschlag et al. 2010; Barros et al. 2013). In

addition, juvenile Haemulon spp. are one of the most

abundant reef fish that are associated with the mac-

roalgal beds in the reef complex of the present study

(Chaves et al. 2013), using these areas as nursery and

feeding grounds.

Although all species preyed upon similar prey

types, the proportion of each prey type in the diet

differed significantly among grunt species. A reduc-

tion in species food overlap is fostered by morpho-

logical differences associated with feeding; in

particular mouth position, shape, and size (Hugueny

and Pouilly 1999; Ward-Campbell et al. 2005).

Consequently, differences in the morphology of

Haemulon species are an important factor in ensuring

food partitioning. Grunts are one of the most diverse

and abundant fish on South Atlantic reefs. Despite this,

little is known about the correlation between ontogeny

and morphological and morphometric changes. Addi-

tionally, the concept of temporal niche partitioning,

proposed by Armstrong and McGehee (1976) could be

relevant. The authors hypothesized that similar food

resources could be exploited by all Haemulon species,

however the species may exploit each resource at

different times. For example, H. parra individuals are

more active during the night than other grunt species

(PHC Pereira, personal observation). Also, Nagelker-

ken et al. (2000) noted that Haemulon spp. forage in

mangroves and seagrass beds at night. The majority of

the species are primarily nocturnal, however it is

unclear what proportion of time they spend feeding

during the day and night (Hobson 1974; Starck and

Davis 1966).

Resource competition (e.g., food and space) within

the four sympatric Haemulon species is likely. This

process is highlighted by a high percentage of

agonistic interactions among them (Pereira and Ferre-

ira 2012) and also by the foraging and behavioural

similarities (Pereira et al. 2010; Pereira and Ferreira

2013). The morphological and ecological transitionsTa

ble

4co

nti

nu

ed

Sp

ecie

sL

ife

ph

ase

Hab

itat

Die

t—m

ost

rele

van

t

item

s(%

vo

lum

e)

Sit

eR

efer

ence

s

Ad

ult

Co

ral

reef

sB

raq

uiu

ra—

26

.9/B

ival

via

—1

4.5

Atl

anti

c—C

arib

bea

n—

Wes

tIn

die

sR

and

all

(19

67

)

Ha

emu

lon

squ

am

ipin

na

Juv

enil

eC

ora

lre

efs

Co

pep

od

a—2

7.1

/Tan

aid

acea

—2

8.1

Atl

anti

c—B

razi

lian

Co

ast

Pre

sen

tst

ud

y

Ad

ult

Co

ral

reef

sP

oly

chae

tes—

30

.5/B

raq

uiu

ra—

28

.4A

tlan

tic—

Bra

zili

anC

oas

tP

rese

nt

stu

dy

Ha

emu

lon

stri

atu

mJu

ven

ile

Co

ral

reef

sC

op

epo

da—

17

.1/C

rust

acea

nL

arv

ae1

0.5

Atl

anti

c—C

olo

mb

ia(S

anta

Mar

ta)

Est

rad

a(1

98

6)

Ad

ult

Co

ral

reef

sB

raq

uiu

ra—

56

.0/P

oly

chae

tes—

11

.5A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)

Ha

emu

lon

stei

nd

ach

ner

iJu

ven

ile

Co

ral

reef

sC

op

epo

da—

47

.1A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)

Ad

ult

Co

ral

reef

sG

astr

op

od

s—2

5.2

/Bra

qu

iura

—1

6.0

/A

tlan

tic—

Co

lom

bia

(San

taM

arta

)E

stra

da

(19

86

)


123


between larval and juvenile life history stages are

more complicated in grunts than in many other reef

fish families (Lindeman et al. 2001) due close

similarity among grunt species (Lindeman 2006).

Moreover, the recruitment and settlement of Haemu-

lon species is influenced by multiple factors such as

depth, predation, and conspecifics presence (Jordan

et al. 2012). Consequently, recruitment success can

change dramatically among species and sites, causing

differences in the abundance of adults of sympatric

species, thus influencing competition levels.

Results from our review suggest that, despite

changes in their habitat use (e.g., coral reefs, man-

groves, or seagrass beds), species of the genus

Haemulon share similar trends in terms of the

ontogeny of their diet. Small crustaceans were the

dominant food item in the stomach contents of

juveniles whereas crabs and polychaetes were domi-

nant in the stomachs of adults at different locations in

the Atlantic Ocean (see Table 4). Moreover, this

review also highlights the fact that most feeding

studies on grunts have been performed in the Carib-

bean (75 %), despite the extreme ecological, econom-

ical, and social importance of grunts in NE Brazil. For

instance, individuals of H. squamipinna and H.

aurolineatum are extensively fished by traditional

communities in the NE Brazil, including in the area

sampled in this study (Fredou et al. 2006; PHC Pereira,

personal observation).

Understanding how similar species coexist is a

central goal of community ecology. Consequently,

several different theories suggest alternative mecha-

nisms to justify the coexistence of spectacularly high

reef fish richness. The lottery hypothesis, (Sale 1977,

1978; Munday 2004.) and neutral model (Bell 2000;

Hubbell 2001) challenge the classic and widespread

niche-partitioning theory which predicts that compe-

tition between species leads to resources partitioning,

with species using a different range of resources in the

presence of a competitor than they do in the absence of

the competitor (Colwell and Fuentes 1975; Schoener

1982; Grant 1986). In this context, reef fishes, such as

the Haemulidae used in the present study, are impor-

tant models to infer how different resource exploita-

tion (i.e., food items), alternative habitat use and also

different morphology and anatomy are likely to ensure

the coexistence of similar ecological species on coral

reefs.

In conclusion, the majority of Haemulon species

can be classified as mobile invertebrate feeders, with

evident ontogenetic diet changes. These changes are

likely associated with species habitat use and mor-

phological changes. As grunts are important both as

predators and prey to other reef species (Randall 1967;

Santos and Castro 2003; Munoz et al. 2011), they play

an important trophic role as a key species in the

Atlantic Ocean marine ecosystem. Further work is still

needed to understand the ontogenetic shifts in their

habitat use, migration, and ecomorphology.

Acknowledgments The authors would like to thank L. Chaves,

J. Feitosa, R. Moraes, and D. Medeiros for help with fieldwork and

for improving the manuscript, as well as local fisher Inho e Sandro

veio for help with fish collection. We would also like to thank M.

Jankowski, J. White and J. Johansen for assistance with English

editing and CAPES (‘‘Coordenacao de Aperfeicoamento de

Pessoal de Nıvel Superior’’) for financial support.

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