2003 feeding ecology of the three juvenile phases of the spiny lobster panulirus argus in a tropical reef lagoon

Marine Biology (2003) 142: 855–865
DOI 10.1007/s00227-003-1013-z

P. Briones-Fourza´n Æ V. Castan˜eda-Ferna´ndez de Lara
E. Lozano-A´lvarez Æ J. Estrada-Olivo

Feeding ecology of the three juvenile phases of the spiny lobster
Panulirus argus in a tropical reef lagoon

Received: 26 January 2002 / Accepted: 9 December 2002 / Published online: 12 February 2003
Ó Springer-Verlag 2003

Abstract The three juvenile phases of the spiny lobster
Panulirus argus (algal phase: 5–15 mm carapace length,
CL; postalgal phase: 15–45 mm CL, and subadults: 45–
80 mm CL) occur in the reef lagoon at Puerto Morelos,
Mexico. The algal phase abounds in this lagoon, which
is covered by extensive seagrass–algal meadows, but the
density of postalgal and subadult juveniles is low,
owing to the scarcity of crevice-type shelters suitable
for these phases. The feeding ecology of the three juvenile phases was investigated to examine whether
spatial or temporal differences in food intake, diet
composition, or nutritional condition occurred among
phases and could partially account for the low abundance of the larger juveniles. Juveniles were collected
by divers at night, from January to November 1995,
throughout the mid-lagoon and back-reef zones. Percent stomach fullness, relative weight of the digestive
gland (RWDG, an index of nutritional condition),
percent frequency of occurrence and percent volume of
food categories in the diet were compared between
sexes, juvenile phases, molt stages (postmolt, intermolt,
premolt), seasons, and sampling zones (mid-lagoon and

back-reef zones). Significant differences in stomach
fullness occurred only among molt stages, mainly because postmolt individuals had emptier stomachs. The
main food categories in all juvenile phases were crustaceans (mostly hermit crabs and brachyurans) and
gastropods, but the food spectrum was wide, including
many other animal taxa as well as plant matter. In
June 1995, the epibenthic macrofauna was sampled in
five sites in the lagoon that differed in their amount of
Communicated by P.W. Sammarco, Chauvin
P. Briones-Fourza´n (&) Æ V. Castan˜eda-Ferna´ndez de Lara
E. Lozano-A´lvarez Æ J. Estrada-Olivo
Instituto de Ciencias del Mar y Limnologı´ a,
Unidad Acade´mica Puerto Morelos,
Universidad Nacional Auto´noma de Me´xico,
P.O. Box 1152, 77500 Cancu´n, Q.R. Mexico
E-mail:
Fax: +52-998-8710138

vegetation. The most abundant taxa in all sites were
decapods and gastropods, but density and diversity
measures showed that the distribution of these potential prey taxa for juvenile P. argus was rather patchy.
Diet overlap in juvenile lobsters was high between
sexes, juvenile phases, sampling zones, seasons, and
molting stages, indicating that all juveniles fed on the
same general food categories throughout time. The
only factor that affected the RWDG was the juvenile
phase. RWDG was significantly lower in subadults
than in algal and postalgal phases, suggesting a poorer
nutritional condition in the largest juveniles. This may
be related to the scarcity of suitable shelters for large
juveniles throughout the lagoon, which may preclude

subadults from exploiting food resources in areas of the
lagoon where shelter is limited.

Introduction
The tropical spiny lobster, Panulirus argus (Latreille,
1804), has a highly complex life history. After a protracted oceanic larval phase that may last up to
9 months, the postlarvae (pueruli) of P. argus return to
coastal areas and settle on shallow vegetated habitats
(seagrass, macroalgae, mangroves). The ensuing benthic
phases of P. argus are: algal juveniles (5–15 mm carapace length, CL), postalgal juveniles (15–45 mm CL),
subadults (45–80 mm CL), and adults (>80 mm CL).
Ontogenetic changes in habitat requirements and social
behavior occur along these benthic phases (reviews in
Butler and Herrnkind 1997, 2000). Algal juveniles remain in shallow, vegetated areas, are solitary, and have
restricted foraging areas. Postalgal juveniles also occur
in shallow habitats, but occupy crevice-type shelters, and
become socially gregarious. Subadults, which retain
gregariousness, have a wider foraging range and occupy
larger crevices, eventually moving towards the reef
habitat.


856

P. argus is one of the most valuable fishing resources
along the Caribbean Sea and the southern Atlantic coast
of the USA (Holthuis 1991). In Mexico, it is heavily
exploited on the coast of the state of Quintana Roo
(eastern margin of the Yucatan Peninsula). However,
some lobster fishing grounds along this coast are very

productive, whereas in others legal-sized P. argus
(‡135 mm abdominal length, i.e. ca. ‡75 mm CL) are
rather scarce. The lobster fishing grounds around Puerto
Morelos (20°51¢N; 86°53¢W; Fig. 1a) are among the
latter (Padilla-Ramos and Briones-Fourza´n 1997), despite high indices of postlarval influx into the Puerto
Morelos reef lagoon (Briones-Fourza´n 1994). To investigate the possible causes for this paradox, the population density, shelter resources, and feeding ecology of
the juvenile phases in this reef lagoon were concurrently
investigated. Densities of algal juveniles in the Puerto
Morelos reef lagoon were estimated as 150–270 individuals ha)1 (Briones-Fourza´n and Lozano-A´lvarez
2001a), but monthly densities of postalgal juveniles and
subadults averaged only 3–8 individuals ha)1 (BrionesFourza´n and Lozano-A´lvarez 2001b). Lack of shelter
resources was found to produce a bottleneck effect at the
postalgal–subadult phases (Briones-Fourza´n and Lozano-A´lvarez 2001b). In the current paper, we present
results on the study of the feeding ecology of all juvenile
phases. This study was conducted to characterize their
diet and to determine whether significant changes in
food intake, diet composition, or nutritional condition
occurred among juvenile phases or in time.
Knowledge of natural diet in an animal species is
essential for studies on its nutritional requirements, its
interactions with other organisms, and its potential for
culture (Williams 1981). General characterizations of the
diet of the different benthic phases of P. argus have been
Fig. 1 a Location of Puerto
Morelos on the eastern margin
of the Yucatan Peninsula,
Mexico. b The Puerto Morelos
reef lagoon. Dotted lines delimit
area of the lagoon where
juveniles of Panulirus argus

were collected. Large dots
indicate the five epibenthic
sampling sites

conducted throughout the geographic range of this
species (e.g. Herrnkind et al. 1975; Andre´e 1981; Marx
and Herrnkind 1985; Colinas-Sa´nchez and BrionesFourza´n 1990; Herrera et al. 1991; Lalana and Ortiz
1991; Cox et al. 1997), but our study is the first to
compare the feeding ecology and nutritional condition
of the three juvenile phases of P. argus in one location.
We did not expect differences in the variables examined
due to sex, juvenile phase, or sampling zone, because
female and male juveniles of spiny lobsters exhibit similar patterns of movement, behavior, and growth
(Andre´e 1981; Joll and Phillips 1984; Butler and
Herrnkind 2000), and all three juvenile phases occur
throughout the Puerto Morelos reef lagoon. Neither did
we expect a strong seasonal effect, because the difference
in mean water temperature in this reef lagoon between
summer and winter is 5–6°C (Merino and Otero 1991;
Ruiz-Renterı´ a et al. 1998). We did, however, expect
differences due to molt stage (postmolt, intermolt, and
premolt), because the molt cycle is known to cause
changes in foraging and feeding activities in some
decapods, including lobsters (Conan 1985; Jernakoff
et al. 1993; de Lestang et al. 2000; Mantelatto and
Christofoletti 2001). We also sampled the epibenthic
fauna of the reef lagoon to assess its composition, as well
as the abundance and distribution of potential prey taxa
for juvenile P. argus.

Materials and methods
Study site
The shallow Puerto Morelos reef lagoon (<1–5 m in depth) extends from the coastline to a coral reef that lies at a distance of ca.
500–2,000 m from the coast (Fig. 1b). The bottom of the lagoon is


857
mostly calcareous sand, covered by extensive seagrass–algal
meadows. Based on its vegetation, the reef lagoon has been divided
into three zones (van Tussenbroek 1995; Ruiz-Renterı´ a et al. 1998;
Monroy-Vela´zquez 2000; Briones-Fourza´n and Lozano-A´lvarez
2001a, 2001b): (1) a narrow coastal fringe, 20–50 m wide, dominated by seagrass (either Syringodium filiforme or Thalassia
testudinum); (2) a broad, densely vegetated mid-lagoon zone, 400–
1,000 m wide, dominated by long-bladed T. testudinum with some
S. filiforme and macroalgae, particularly the brown alga Lobophora
variegata; and (3) a poorly vegetated back-reef zone, 100–400 m
wide, with variable densities of short-bladed T. testudinum and
rhizophytic macroalgae, and a virtual absence of S. filiforme and
L. variegata. All three juvenile phases of P. argus occur throughout
the mid-lagoon and back-reef zones (Briones-Fourza´n and LozanoA´lvarez 2001a, 2001b). Mean water temperatures in the reef lagoon
during 1995, estimated from daily measurements taken at
~0900 hours at a depth of 0.5 m, were 24.50°C in the winter
(January–February), 27.22°C in the spring (March–May), 29.41°C
in the summer (June–August), and 28.54°C in the autumn
(September–November).

Sampling of juvenile lobsters
Juvenile lobsters were obtained by hand, using SCUBA diving. To
minimize the error introduced into estimates of dietary importance
by differential digestion (Herrnkind et al. 1975; Williams 1981), we

collected juveniles between 2000 and 2300 hours, i.e. during their
period of peak feeding (Andre´e 1981; Castan˜eda 1998). Because of
the low densities of the postalgal and subadult phases, divers collected juveniles throughout the mid-lagoon and back-reef zones
(Fig. 1b), whether they were foraging or not, in order to obtain
samples of reasonable sizes. Samples were taken during the dark
lunar phases from January to November 1995, and data were
compiled for season. In the winter, some juveniles were also collected in pre-dawn hours (0400–0530 hours) (Joll and Phillips 1984)
to increase sample size. To ascertain whether the collection of these
few individuals would affect the results, we compared the number of
individuals with <50% and >50% of gut fullness between the two
sampling times. The results of the tests were not significant (v2=
0.0417, df=1, P>0.75). After collection, juveniles were individually
introduced into numbered bags and placed on ice to slow digestion.
Transportation by boat to the Puerto Morelos Academic Unit of
the National Autonomous University of Mexico (Fig. 1) took
about 1 h. There, juveniles were stored at )4°C and their stomach
contents were sorted and fixed the morning following their capture.

Laboratory analysis
The following data were recorded from each lobster: sex, sampling
zone (mid-lagoon or back-reef zone), carapace length (CL,
±0.1 mm, measured from between the rostral horns to the posterior margin of the cephalothorax), and total weight (TW, ±0.1 g,
after blotting the excess water). Individuals were classified as
postmolt, intermolt, or premolt, based on the determination of
their stage in the molt cycle after observation of a pleopod under a
microscope (Lyle and MacDonald 1983). Lobsters were then dissected to extract their stomach and digestive gland. The digestive
gland was blotted and weighed (WDG, ±0.01 g), and its relative
weight (RWDG=WDG/TW·100) was obtained as an index of the
nutritional condition of individuals. Starved or poorly fed individuals have significantly lower values of RWDG than well-fed
individuals (Dall 1974).

The percent fullness of the stomach was visually calculated and
categorized according to the following scale: 0% (0–5%), 10% (6–
15%), 25% (16–35%), 50% (36–65%), 75% (66–90%) and 100%
(91–100%) full. Although visual estimations of gut fullness are
subjective, they have the advantage of being simple and rapid to
apply, and provide a reasonably reliable means to determine differences in gut fullness between individuals of the same species

independent of their size (Hyslop 1980), particularly in decapods
(Williams 1981; Cartes and Sarda` 1989; Jernakoff et al. 1993; de
Lestang et al. 2000; Mantelatto and Christofoletti 2001; Oh et al.
2001), because in decapods the gut wall is not as distensible as in
fishes and places a relatively uniform limit on the maximum gut
volume (Maller et al. 1983). Diet analysis was conducted only on
those juveniles with their stomachs ‡10% full (Joll and Phillips
1984; Jernakoff et al. 1993). Stomach contents were sorted under a
stereomicroscope to the lowest taxonomic level possible. Some
items were identified to species, but most were identified to higher
levels due to their fragmentation and/or partial digestion. Contents
were grouped for data analysis in food categories corresponding to
gross taxa. Percent frequency of occurrence (%F=the number of
stomachs containing a given food category/total number of stomachs examined·100) was determined for each food category.
Frequency of occurrence provides a rather qualitative picture of
the food spectrum, because it does not take into account the relative contribution to the diet of food items of different sizes. Statistical comparisons are sounder when applied to quantitative
measures, taking into account the bulk of food items (Hyslop 1980;
Williams 1981). Hence, we estimated the percent volume of each
food category in the stomach contents. To avoid the subjectivity
associated with estimating the percent volume of food categories by
eye, the food categories of an individual stomach were placed on a
large Petri dish and squashed to a uniform depth. The Petri dish
had a disk of millimetric paper glued to its exterior. The area (i.e.

number of squares) for each food category, measured under a
magnifying glass, was used to estimate its percent contribution by
volume (%V) to the total volume of stomach contents, which was
the sum of the areas of all food categories. This technique standardizes the volume estimates irrespective of the size of the lobsters
(Hyslop 1980; Joll and Phillips 1984).

Data analysis
Contingency table analyses were employed to test the association
between stomach fullness and the following five factors: sex (male
and female), juvenile phase (algal, postalgal and subadult), molt
stage (postmolt, intermolt, and premolt), season (winter, spring,
summer, and autumn), and sampling zone (mid-lagoon and backreef zone) (Oh et al. 2001).
To fully explore the effects and interaction terms of the five
above-mentioned factors on the nutritional condition (RWDG) of
juvenile P. argus, a five-factor ANOVA would be in order, but the
data were insufficient to fill all the resulting cells. However, within
the framework of our study the most important effects to explore
on the nutritional condition of juvenile P. argus were those of
season, juvenile phase, and molt stage compared to those of sex and
sampling zone, because sex has no apparent effect on the foraging
movements and general behavior in juveniles of P. argus and other
palinurids (Andre´e 1981, Joll and Phillips 1984; Jernakoff et al.
1993; Butler and Herrnkind 2000) and the majority of our individuals were collected in the mid-lagoon. Therefore, we excluded
sex and sampling zone from the factorial analysis and ran independent Student’s t-tests on each of them. We then ran a threefactor ANOVA with season (four levels: winter, spring, summer
and autumn), juvenile phase (three levels: algal, postalgal, and
subadults), and molt stage (two levels: intermolt and premolt) as
fixed factors. We did not include postmolt individuals in the
analysis because these made up only 10% of all individuals.
Pairwise diet overlap indices were estimated between levels of
each factor by means of Horn’s overlap index (Horn 1966), applied

to the values of %V. When diet overlap is compared between intraspecific groups, index values £ 0.8 are considered to be indicative of major differences (Cartes and Sarda` 1989; Oh et al. 2001).
Pairwise comparisons of the %F of food categories were also made
using Spearman’s non-parametric rank correlation test (Fritz 1974;
Williams 1981; Lalana and Ortiz 1991; Drazen et al. 2001; Oh et al.
2001). To reduce the effect of rare groups on the correlations, only
food categories that constituted %F>10 were included in comparisons (Drazen et al. 2001).


858
Study of the epibenthos
We sampled the epifauna in five sites throughout the reef lagoon
(Fig. 1b) to assess the composition, abundance, and distribution of
potential prey taxa for juvenile P. argus. Sites 1–3 (depth range:
3.0–3.5 m) were located in the densely vegetated mid-lagoon zone,
whereas sites 4 and 5 (depth: 4 and 3 m) were located in the poorly
vegetated back-reef zone.
We sampled the epibenthic macrofauna by means of an epibenthic sleigh-net. This method would result in an undersampling
of fast-moving, strongly attached, or infaunal species, but we used
it because the diet of juvenile and adult P. argus is mostly composed of slow-moving, epibenthic macrofauna, particularly decapod and gastropod species (Herrnkind et al. 1975; Colinas-Sa´nchez
and Briones-Fourza´n 1990; Herrera et al. 1991; Cox et al. 1997).
The mouth of the net measured 0.57 m width·0.25 m height and
the mesh aperture was 1 mm. In seagrass habitats, night samplings
yield significantly more species and individuals than day samplings,
because of the nocturnal habits of many of the species in the
epifauna (Heck 1977; Estrada-Olivo 1999; Monroy-Vela´zquez
2000). Therefore, we obtained ten net trawls in each of the five
sampling sites (i.e. 50 trawls) between 2000 and 2200 hours, on 20–
24 June 1995. Successive trawls in each site were conducted in such
a way as to avoid going over the same place twice. Each trawl had a
duration of 1 min at a speed of 1 m s)1, and was visually monitored

by a diver to ensure that the net performed properly. The average
area covered by the ten trawls in each sampling site was $342 m2
(Briones-Fourza´n and Lozano-A´lvarez 2001a).
Organisms from the ten trawls in each site were identified to
species, quantified, and standardized as number of individuals per
hectare. The relative abundance of similar taxa among sites was
compared with a Kruskall–Wallis non-parametric ANOVA (Zar
1984). Distribution and diversity of crustacean and mollusk assemblages in each site were established using the following indices
(Gray 2000): (1) species richness, S=the number of species; (2)
heterogeneity diversity, HD=exp(H ¢), where H ¢ is the commonly
used Shannon–Wiener index; (3) evenness, J¢=H ¢–Hmax, where
Hmax is maximal diversity (lnS), and (4) dominance, d=Nmax/N,
where Nmax is the number of individuals in the most abundant
species and N is the total number of individuals. Natural logarithms were used in all indices.

Results
Natural diet and nutritional condition
of juvenile Panulirus argus
In total, we caught 182 juveniles (size range: 11.1–
80.0 mm CL), of which 78 were females and 104 males.
Most individuals (144) were collected in the mid-lagoon
zone, and 38 in the back-reef zone. By phase, 47 juveniles were algal, 91 postalgal, and 44 subadults, whereas
by molt stage 19 were in postmolt, 76 in intermolt, and
87 in premolt. The proportion of juveniles in the three
molt stages was similar in all seasons (v2=7.652, df=6,
P>0.25). No significant differences in stomach fullness
occurred between sexes, juvenile phases, seasons, or
sampling zones, but significant differences occurred
among molt stages (Fig. 2). This was due to the large
proportion of postmolt juveniles with <10% stomach

fullness.
The relative weight of the digestive gland was estimated in 176 individuals. As expected, there were no
effects on the RWDG of either sex (mean±SE of females: 4.11±0.10; of males: 4.40±0.11; t=1.652,

df=175, P>0.1) or sampling zone (in mid-lagoon zone:
4.32±0.09; in back-reef zone: 4.16±0.13; t=0.536,
df=175, P>0.5). Results of the three-factor ANOVA
showed that the only factor with a significant effect on
RWDG was juvenile phase (Tables 1, 2). A post hoc
Tukey comparison test for samples of unequal sizes (Zar
1984) showed that the mean RWDG of subadults
(3.80±0.11) was significantly lower than the mean
RWDG of algal (4.49±0.16) and postalgal juveniles
(4.39±0.11), suggesting that subadults were in a poorer
nutritional condition than the remaining juvenile phases
(Table 1). The lack of first- or second-order interactions
(Table 2) indicates that the mean RWDG was consistently lower in subadults.
The most distinct components of the stomach contents of juvenile P. argus in all four seasons were crustaceans (pieces of appendages, eyes, carapace fragments)
and gastropods (fragments of shells, opercula) (Table 3).
Crustacean prey were mostly hermit crabs of the families
Paguridae and Diogenidae, and brachyuran crabs of the
families Majidae and Xanthidae. Recognizable gastropod prey included species of the families Trochiidae,
Neritidae, Cerithiidae, Modulidae, and Fasciolariidae.
Other animal food categories were bivalves (fragments
of shells), chitons (plates), sponges (spongine, spicules),
echinoderms (spines, calcified fragments), polychaetes
(mandibles, body pieces), barnacle postlarvae, foraminifers, and remains of tunicates, bryozoans, and corals.
Plant food categories comprised pieces of seagrass
blades and macroalgae, as well as coralline algae. Although not a food category, sediment was an abundant
component of the stomach contents, both in %F and

%V. Similarly, soft matter (a mixture of partially digested soft body parts of unidentified prey items) was
also abundant, even though samplings were conducted
during the peak in feeding activity.
The number of food categories in individual stomachs ranged from 4 to 14. Because of the differential
digestion of food types, Williams (1981) recommended
the use of individuals with stomachs ‡50% full to obtain
the most accurate data on types of food ingested. We
found significant differences in the mean number of food
categories between individuals with stomach fullness
<50% (mean±SE: 6.1±0.25, n=46) and ‡50%
(8.7±0.20, n=105) (Student’s t-test: t=7.699, df=149,
P<0.001). However, since our juveniles were collected
in their peak feeding period, our <50% full animals
(30% of the total) may reflect juveniles that started
feeding later, or that had low feeding rates, rather than
individuals in an advanced stage of digestion (Joll and
Phillips 1984).
Diet overlap
Table 4 summarizes the values of Horn’s overlap indices
and Spearman’s rank correlation coefficients between all
pairwise comparisons. Virtually all correlation coefficients were significant, and all the values of Horn’s index


859
Fig. 2a–e Juvenile Panulirus
argus. Degree of stomach
fullness compared by: a sex, b
juvenile phases, c molt stages, d
seasons, and e sampling zones.
Results of contingency table

analysis (v2) appear below each
graph (df degrees of freedom).
Numbers above bars represent
sample sizes

were >0.8, indicating a high diet overlap in juveniles of
P. argus regardless of the factor explored. The lowest
Horn’s indices occurred in some seasonal comparisons:
between autumn and winter (0.814), spring and autumn
(0.876), and winter and summer (0.903), reflecting seasonal changes in the relative volumetric composition of
Table 1 Juvenile Panulirus argus. Mean (±SE) of relative weight
of digestive gland (RWDG: weight of digestive gland/weight of
whole animal·100) of individuals grouped by factors and levels
explored in a three-factor ANOVA (see Table 2)
Factor

Levels

N

RWDG

Molt stage

Intermolt
Premolt
Winter
Spring
Summer
Autumn

Algal
Postalgal
Subadult

72
86
47
49
36
45
46
91
40

4.30±0.13
4.35±0.10
4.12±0.17
4.31±0.16
4.42±0.10
4.33±0.13
4.49±0.16
4.39±0.11
3.80±0.11

Season

Juvenile phase

food categories (see Table 3), but still indicating an
overall high diet overlap among seasons.

Epifauna in the reef lagoon
In all, 173 epifaunal species were identified, of which 79
were crustaceans and 48 mollusks (Table 5). The rest
Table 2 Juvenile Panulirus argus. Results of the three-factor
ANOVA (fixed factors) on log-transformed data (see Table 1)
Effect

df

A: Molt stage
B: Season
C: Juvenile phase
A·B
A·C
B·C
A·B·C
Error

1
3
2
3
2
6
6
135

Mean square

F-value

0.274
0.084
4.249
0.669
0.319
0.465
0.536
0.866

0.315
0.097
4.906
0.772
0.369
0.537
0.618

P
0.575
0.962
0.009
0.512
0.692
0.780
0.715


860
Table 3 Juvenile Panulirus

argus. Percent frequency of
occurrence (%F) and percent
volume (%V) of food categories
by season. In parentheses,
number of juveniles examined
(i.e. juveniles with their
stomachs at least 10% full) in
each season

Table 4 Juvenile Panulirus
argus. Horn’s diet overlap index
values based on percent volume
(%V) of food categories (+,
high overlap) and Spearman’s
correlation coefficients based on
percent frequency (%F) of food
categories (n.s. not significant;
*P<0.05, **P<0.01,
***P<0.001) compared by sex,
juvenile phase, molt stage,
season, and sampling zone.
Reef lagoon at Puerto Morelos,
Mexico

Food categories

Crustaceans
Gastropods
Plant matter
Sediment

Soft matter
Sponges
Bivalves
Calcareous algae
Echinoderms
Foraminifers
Tunicates
Fish
Barnacle postlarvae
Polychaetes
Bryozoans
Chitons
Coral

Factor

Winter (34)

Spring (41)

Summer (37)

Autumn (39)

%F

%V

%F

%V

%F

%V

%F

%V

88.2
88.2
70.6
70.6
82.4
47.1
38.2
14.7
2.9
41.2
5.9
5.9
2.9
0
0
0
0

30.4
14.5

4.4
11.9
14.8
16.5
2.7
0.9
0.4
0.8
2.0
0.5
0.2
0
0
0
0

92.7
92.7
48.8
61.0
82.9
48.8
41.5
14.6
2.4
39.0
0
0
9.8
17.1

2.4
4.9
0

43.4
19.4
2.7
3.7
15.0
7.9
3.8
0.2
0.1
0.3
0
0
1.4
1.1
0.5
0.5
0

91.9
89.2
67.6
70.3
97.3
16.2
2.7
8.1

5.4
40.5
0
5.4
5.4
21.6
0
8.1
5.4

34.4
22.1
4.5
7.3
24.2
2.4
0.2
0.1
1.4
0.5
0
0.3
0.1
1.8
0
0.4
0.4

94.9
94.9

53.8
97.4
100.0
12.8
12.8
18.0
46.1
64.1
0
7.7
0
41.0
0
35.9
30.8

36.8
16.4
1.8
6.0
15.5
0.8
1.0
0.2
13.0
0.6
0
0.2
0
4.3

0
3.4
0.1

Pairwise comparison

Sex
Females vs. males
Juvenile phase Algal vs. postalgal
Postalgal vs. subadult
Algal vs. subadult
Molt stage
Postmolt vs. intermolt
Intermolt vs. premolt
Premolt vs. postmolt
Season
Winter vs. spring
Spring vs. summer
Summer vs. autumn
Autumn vs. winter
Spring vs. autumn
Winter vs. summer
Sampling zone Mid-lagoon vs. back-reef

included species of fishes, polychaetes, echinoderms,
sponges, and other taxa. Decapod crustaceans and gastropod mollusks were the most abundant taxa in the
epifauna, with 63 and 36 species, respectively. Sites 1–3
had more crustaceans per unit area than sites 4 and 5
(Table 5), but the relative densities of the different taxa
of crustaceans did not vary significantly among sites

(Kruskall–Wallis test: H=4.727, df=4, P=0.317), nor
did those of the mollusk taxa (H=2.983, df=4,
P=0.561). The highest densities of mollusks occurred in
sites 1 and 4, and the lowest in sites 2 and 5 (Table 5).
Overall, the most numerous decapods in the reef lagoon (the most abundant species following in parentheses) were caridean shrimps of the families
Hippolytidae (Latreutes fucorum, Thor manningi) and
Palaemonidae (Periclimenes americanus), followed by
hermit crabs of the families Paguridae (Pagurus annulipes, P. brevidactylus) and Diogenidae (Clibanarius tricolor). Brachyurans were less abundant, and were mostly
represented by majids (Mithraculus sculptus, M. forceps,
Pitho aculeata), portunids (Portunus spp.), and xanthids
(Panopeus occidentalis). Among the mollusks, the most
abundant families were Phasianellidae (Tricolia sp.),
Cerithiidae (Cerithium litteratum, Cerithium sp.), and

Horn’s overlap index Spearman’s correlation coefficient
0.973
0.978
0.969
0.950
0.907
0.986
0.918
0.930
0.942
0.928
0.814
0.876
0.903
0.945

(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)
(+)

0.952***
0.917**
0.830**
0.900**
0.768*
0.935**
0.775**
0.971***
0.875**
0.945***
0.708n.s.
0.634*
0.893**
0.618**

Trochidae (Tegula fasciata). The epifaunal taxa that
were represented in the gut contents of juvenile P. argus
are also indicated in Table 5 by asterisks.
Table 6 shows the diversity measures estimated for
the crustacean and mollusk assemblages, as well as some
characteristics of the vegetation (taken from BrionesFourza´n and Lozano-A´lvarez 2001a) in each sampling
site. The abundance of crustaceans was highest in more
vegetated sites (1–3) than in less vegetated sites (4 and 5).
The largest number of species (S) and individuals (N)
occurred in site 3, but dominance was lowest in this site,
because the four most numerous species (L. fucorum,
P. americanus, T. manningi, and P. annulipes) all had
similar numbers of individuals. The lowest diversity and
greatest dominance occurred in site 4, where two species
(P. annulipes and L. fucorum) comprised >66% of
individuals. In contrast, S was large relative to N in
site 5, yielding high diversity and low evenness. Sites 1
and 2 had intermediate values of all diversity measures
(Table 6).
Unlike crustaceans, the abundance of mollusks was
apparently not related to the degree in vegetation
(Table 6). In site 1, mollusk abundance and diversity
were highest, but dominance was least, owing to the


861
Table 5 Density estimates of
the distinct taxa of
macrobenthic epifauna
collected in five sites in the

Puerto Morelos reef lagoon.
Ten epibenthic net trawls, 60 m
long on average, were made at
each site during the night
(trawled area per site ~342 m2).
Numbers in parentheses are
number of species identified in
each taxon. Asterisks denote
those taxa that were represented
in stomach contents of juvenile
Panulirus argus

Table 6 Summary of diversity
measures of crustacean and
mollusk assemblages in five
sampling sites, reef lagoon at
Puerto Morelos, Mexico,
during the summer of 1995. The
vegetation characteristics were
taken from Briones-Fourza´n
and Lozano-A´lvarez (2001a).
Seagrass and macroalgal
densities are number of blades
or thalli per square meter;
biomass of the brown drift alga
Lobophora variegata is grams of
dry weight per square meter

Density (individuals ha)1) per site

Taxon

Crustacea (79)
Stomatopoda (2)*
Amphipoda (2)*
Isopoda (8)*
Penaeidae (1)
Sicyoniidae (2)
Palaemonidae (3)
Alpheidae (4)*
Hippolytidae (7)
Processidae (3)
Palinuridae (1)
Diogenidae (9)*
Paguridae (4)*
Majidae (16)*
Portunidae (2)*
Xanthidae (11)*
Other decapods (4)*
Mollusca (48)
Trochidae (3)*
Turbinidae (2)
Phasianellidae (1)*
Neritidae (1)*
Modulidae (1)*
Cerithiidae (2)*
Crepidulidae (2)
Epitoniidae (1)
Columbellidae (1)*
Nassariidae (1)

Other gastropods (21)*
Bivalvia (8)*
Other molluscs (4)*
Other taxa (46)
Polychaeta (6)*
Echinodermata (6)*
Porifera (4)*
Pisces (25)*
Other (5)*
Total taxa (173)

Assemblage

Crustaceans

Mollusks

Vegetation

Average

Site 1

Site 2

Site 3

Site 4

Site 5

190,146
556
88
1,082
322
468
40,994
8,450
70,819
4,152
263
7,573
51,433
2,193
1,053
673
29
119,268
23,421
8,246
21,813
2,368
10,029
47,310
234
409
673
1,140
2,544

731
350
7,894
88
205
0
7,544
58
317,308

130,263
614
58
1,404
673
702
39,942
5,643
67,018
8,012
117
205
4,942
468
351
117
0
43,129
5,965
3,129

14,708
994
6,784
10,526
58
0
234
88
556
88
0
4,123
0
0
0
4,123
0
177,515

285,789
702
117
1,462
731
1,082
55,000
10,146
137,339
9,094
146

3,626
62,076
2,661
1,053
378
175
87,105
10,439
2,982
43,830
1,433
8,187
13,216
205
234
1,901
2,924
1,579
146
29
5,585
117
205
0
5,234
29
378,479

112,953
0

205
146
88
760
6,374
0
38,450
3,041
29
4,942
56,228
2,339
351
0
0
106,404
526
614
70,906
2,632
789
6,082
0
673
15,731
6,082
2,339
29
0
2,309

0
58
1,199
994
58
221,666

68,742
439
292
906
88
1,930
4,386
2,544
32,193
8,538
175
175
14,532
1,988
292
117
146
66,024
1,959
497
43,246
234
3,187

3,801
205
175
7,982
994
3,187
351
205
1,316
468
468
88
146
146
136,082

Characteristics

Sampling site

Species richness (S)
Number of individuals (N)
Diversity (HD)
Evenness (J¢)
Dominance (d)
Species richness (S)
Number of individuals (N)
Diversity (HD)
Evenness (J¢)
Dominance (d)

Seagrass density
Macroalgal density
Biomass of L. variegata

large N-values of four species (Cerithium litteratum,
Cerithium sp., Tegula fasciata, and Tricolia sp.). In
contrast, Tricolia sp. comprised 66% of all individuals in
sites 4 and 5, producing low diversity and high dominance indices.

157,579
462
152
1,000
380
988
29,339
5,357
69,164
6,567
146
3,304
37,842
1,930
620
257
70
84,386
8,462
3,094
38,901

1,532
5,795
16,187
140
298
5,304
2,246
2,181
269
117
4,246
135
187
257
3,608
58
246,211

1

2

3

4

5

51
6,512

9.545
)1.676
0.236
32
4,079
8.281
)1.352
0.201
639.2
72.0
25.0

37
4,455
7.434
)4.605
0.314
19
1,487
7.036
)0.993
0.338
560.0
211.8
24.7

62
9,775
9.934
)1.831

0.196
28
2,978
6.178
)1.511
0.503
507.2
107.6
5.0

36
3,864
6.246
)1.752
0.344
24
3,639
3.387
)1.958
0.666
0
103.2
0

53
2,351
12.158
)1.472
0.283
25

2,253
4.154
)1.795
0.656
198.4
109.4
0

Discussion
The diet of juvenile Panulirus argus included a wide
food spectrum, similar to the diet of adult P. argus


862

(Herrnkind et al. 1975; Colinas-Sa´nchez and BrionesFourza´n 1990; Herrera et al. 1991; Cox et al. 1997) and
of many other palinurid species (Lindberg 1955; Berry
1971; Newman and Pollock 1974; Joll and Phillips 1984;
Barkai and Branch 1988; Edgar 1990; Jernakoff et al.
1993; Lozano-A´lvarez and Aramoni-Serrano 1996).
Based on their wide food spectrum, palinurids have been
classified as generalist feeders, and based on their feeding behavior as ‘‘searchers’’, i.e. animals that are
opportunistic, have wide diets, and feed predominantly
on small prey (Andre´e 1981; Joll and Phillips 1984;
Jernakoff et al. 1993).
Molt frequency in most decapods decreases as size
increases; consequently, juvenile P. argus molt many
times in a year (Lozano-A´lvarez et al. 1991; Forcucci
et al. 1994). This reduces the length of the intermolt
period compared to the length of the premolt period (Oh

et al. 2001), and was reflected in the similar numbers of
intermolt and premolt juveniles in our samples. In contrast, postmolt juveniles accounted for only 10% of our
total sample, and had significantly more empty stomachs
than intermolt or premolt juveniles. Recently molted
juveniles tend to remain hidden in their crevices and
were probably less vulnerable to the sampling technique.
Also, postmolt individuals tend to have emptier stomachs, because their mouthparts are not yet sufficiently
hardened to allow them to feed (Herrera et al. 1991;
Jernakoff et al. 1993).
The diet of male and female juvenile P. argus was
virtually the same. This is common in juvenile palinurids, because there are no differences in foraging behavior
between juvenile males and females (Joll and Phillips
1984; Jernakoff et al. 1993). Similarly, the high diet
overlap between the three juvenile phases of P. argus
suggests that they all forage in similar areas throughout
the Puerto Morelos reef lagoon. Algal juveniles are more
abundant in those vegetated areas of the mid-lagoon
richer in the brown alga Lobophora variegata, but they
also occur in the less vegetated areas of the back-reef
zone (Briones-Fourza´n and Lozano-A´lvarez 2001a).
Crevice-type dens, where postalgal and subadult juveniles seek shelter, are scarce and overdispersed
throughout the lagoon (Briones-Fourza´n and LozanoA´lvarez 2001b). The back-reef zone is richer in den resources for subadults, and the mean size of juveniles
taken from the back-reef zone was indeed larger than the
mean size of those juveniles collected in the mid-lagoon
zone (mean CL±SD in the back-reef zone: 47.5±
18.6 mm; in the mid-lagoon zone: 33.3±11.6 mm; Student’s t-test on log-transformed data: t=4.965, df=180,
P<0.001). Yet, of the total 44 subadults, 45% were
collected in the mid-lagoon, where they were found
foraging close to or denning under piers and in crevices
at minimum distances of only 150 m from the coast.

Therefore, all juvenile phases occurred throughout the
lagoon and were thus presented with the same potential
prey taxa, which was further reflected in the high diet
overlap between the two sampling zones. Similar results
were obtained in individuals over a wide size range of

the swimmer crab Portunus pelagicus caught throughout
one estuary (de Lestang et al. 2000). In contrast, adults
of P. argus, which inhabit the deeper fore-reef and shelf
zones of Puerto Morelos, include more mollusks than
crustaceans in their diet (Colinas-Sa´nchez and BrionesFourza´n 1990).
Most studies on the natural diet of P. argus have been
based on percent frequency of occurrence (%F) of food
categories. In the Virgin Islands, different %F-values
were found for crustaceans and mollusks in gut contents
of P. argus, caught either in mangrove (juveniles) or reef
(adults) habitats (Herrnkind et al. 1975). Similarly, %F
of food items in algal juveniles of P. argus differed
among several Florida Keys (Andre´e 1981; Marx and
Herrnkind 1985). In Florida and Cuba, the most frequent food items in subadult and adult P. argus were
gastropods, followed by crustaceans (Herrera et al. 1991;
Cox et al. 1997), but their %F varied according to the
habitat where they foraged. The most frequent food
categories in our juveniles throughout the year were
crustaceans and mollusks, the most abundant taxa in the
epifauna of the Puerto Morelos reef lagoon. Therefore,
the diets documented for the distinct benthic phases of
P. argus, based on %F, are a reflection of the local
abundance of available potential prey.
The epifauna in the Puerto Morelos reef lagoon was

similar in composition to the epifauna in other shallow
seagrass habitats throughout the Caribbean Sea and
Florida, where crustaceans and mollusks are the most
abundant taxa (e.g. Heck 1977; Heck and Wetstone
1977; Lewis and Stoner 1983; Bell and Westoby 1986;
Lalana et al. 1987). However, the density and diversity
estimates of the epifaunal taxa showed that the distribution of potential prey for juvenile P. argus is highly
patchy, and that some patches may be potentially richer
in food resources than others. Moreover, the diet of our
juvenile P. argus included the most abundant taxa of
mollusks in the epifauna, but the most numerous crustacean taxa (caridean shrimps) were altogether absent in
their guts (see Table 5). As is the general case in palinurids (e.g. Newman and Pollock 1974; Herrnkind et al.
1975; Joll and Phillips 1984; Lalana and Ortiz 1991), the
animal remains in the guts of our juvenile P. argus belonged to slow-moving, sedentary, or sessile organisms,
such as hermit crabs, majids, xanthids, gastropods,
sponges, and echinoderms. Juvenile P. argus may have
difficulty capturing fast-moving prey, such as caridean
shrimps, and hence do not exploit this most abundant
food resource. Remains of fish, which are also fastmoving animals, probably belonged to dead or injured
individuals. Our juveniles also consumed infaunal species, such as small bivalves, polychaetes, and foraminifers, but in low proportions. Palinurids may use the tips
of their first pairs of walking legs to dig in the sediment
for prey (Herrnkind et al. 1975; Joll and Phillips 1984;
Cox et al. 1997), but the low %V of infaunal organisms
and the high %V of sediment in the guts of our juvenile
lobsters suggest that there is little prey selectivity for
infauna, probably because the excavation of infauna


863

requires greater energy than the capturing of slowmoving epifauna (Oh et al. 2001). The low %V of plant
matter suggests that juveniles may have consumed it
incidentally while attempting to capture epifaunal prey,
although in other palinurids certain algae are an important component of the diet (Joll and Phillips 1984;
Edgar 1990).
We only sampled the epifauna during summer, because we did not expect significant seasonal differences
in the diet of juvenile P. argus, which was confirmed by
the high diet overlap indices obtained between seasons.
However, seasonal changes in the abundance of some
taxa of the epifauna could underlie minor seasonal differences in %V and %F of distinct food categories in gut
contents of juveniles. For instance, decapods are less
abundant in the Puerto Morelos reef lagoon in the
winter (Monroy-Vela´zquez 2000), when the lowest %F
and %V of crustaceans occurred in the guts of juvenile
P. argus. Alternatively, the higher %V of sponges in the
winter, and of echinoderms, polychaetes, and chitons in
autumn, may reflect seasonal increases in the availability
of these prey taxa. In Western Australia, significant
seasonal differences in diet, both in small (<25 mm CL)
(Jernakoff et al. 1993) and large (>25 mm CL) (Joll and
Phillips 1984; Edgar 1990) juveniles of P. cygnus, were
related to seasonal changes in the abundance of prey
categories. Moreover, palinurids may switch to uncommon food sources when the abundance of the latter increases and/or when other types of prey are unavailable.
For example, P. cygnus consumed large quantities of
epitokous polychaetes when this unexpected food source
became abundant (Edgar 1990), and Jasus lalandii
preyed on large amounts of mysids and recently settled
barnacles in locations where its more usual prey (mussels) was unavailable (Barkai and Branch 1988). Such
switching is common in polyphagous species, because it
maximizes foraging efficiency when alternative prey

species become more abundant than the preferentially
consumed species (Murdoch and Oaten 1975). Nevertheless, the high diet overlap among seasons indicate
that, despite possible seasonal differences in prey availability, juveniles fed on the same general food categories
throughout the year.
Because starving decreases the solids in the digestive
gland, both the wet and dry weight of the digestive
glands are considered as reliable indicators of the nutritional condition in spiny lobsters (Dall 1974), both in
the laboratory and in the field. For example, Dall (1974)
obtained significantly lower RWDGs (mean±SE:
4.1±0.12) in individuals of P. cygnus experimentally
starved for 4 weeks than in individuals fed ad lib
(5.5±0.38). In Guerrero, Mexico, the digestive glands of
individuals of P. inflatus were in poor condition in the
winter, because a significant increase in the population
density of this lobster during autumn presumably reduced the availability of food in the winter (LozanoA´lvarez and Aramoni-Serrano 1996). However, these
indices have seldom been used, because they involve
killing the animals as well as time-consuming dissections

(Dall 1975; Oliver and MacDiarmid 2001). Since we had
to sacrifice our juveniles in order to dissect their guts, we
preferred to use the RWDG over other, more laborious
biochemical indices of nutritional condition that are
derived from live animals (Dall 1974, 1975; Martinelli
1993; Roberston et al. 2000, Musgrove 2001).
The significantly lower mean RWDG of subadults
suggests that these large juveniles were in poorer nutritional condition than their smaller counterparts, irrespective of season. This was unexpected because, even
though decapods tend to prefer relatively small prey
(Juanes 1992) and the high diet overlap among juvenile
phases suggests intraspecific competition for the same
food categories, the size of prey generally tends to increase with predator size (de Lestang et al. 2000; Drazen

et al. 2001; Mantelatto and Christofoletti 2001; Oh et al.
2001), and this has been confirmed in juvenile P. cygnus
(Edgar 1990) and adult P. argus (Herrera et al. 1991).
Therefore, ontogenetic dietary shifts that are not evident
at high taxonomic levels of prey may occur at the species
level, or according to the size of prey. This may also
apply to the juvenile phases of P. argus in the Puerto
Morelos reef lagoon, but we did not conduct this analysis. Thus, the reasons for the poorer nutritional condition in subadults remain speculative. Food resources
in the reef lagoon may be less abundant, or of a lower
nutritional quality, for these large juveniles. An alternative explanation invokes the scarcity of crevice-type
shelters suitable for subadults throughout the reef lagoon (Briones-Fourza´n and Lozano-A´lvarez 2001b).
The lack of shelter resources increases predation-induced mortality (Smith and Herrnkind 1992) and may
thus restrict the foraging movements of subadults to
minimize their risk of predation, precluding their exploitation of food resources in areas where shelter is
limited, or it may affect their foraging efficiency by increasing the distances these animals need to traverse in
order to forage on rich food patches (Schoener 1971;
Stephens and Krebs 1986).
Poor nutritional condition, as measured with other
indices, can affect growth in P. cygnus (Dall 1975),
Homarus gammarus (Hagerman 1983), and Jasus
edwardsii (Oliver and MacDiarmid 2001), but we do not
know whether the RWDG values of subadult P. argus
obtained in our study are low enough to affect their
growth or mortality. Hence, more experimental and field
investigation is needed to ascertain whether the seemingly poor nutritional condition of subadults, in
conjunction with the lack of appropriate natural shelters
for this benthic stage (Briones-Fourza´n and LozanoA´lvarez 2001b), could also account for the further
scarcity of adult lobsters in the deeper fishing grounds of
Puerto Morelos.
Acknowledgements We acknowledge the help provided by

F. Negrete-Soto in field work and data processing, and by
C. Barradas-Ortiz, G. Reyes-Zavala, E. Cadena-Barrientos, and
P. Rangel-Zarza in field and/or laboratory activities. V. MonroyVela´zquez, E. Cadena-Barrientos, F. Solı´ s, and F. Escobar de la
Llata helped to identify the epifauna. F. Ruiz-Renterı´ a kindly


864
provided the water temperature data. Comments by three anonymous reviewers greatly improved the manuscript. This project
(no. 1171-N) was supported by Consejo Nacional de Ciencia y
Tecnologı´ a (CONACyT-Me´xico), including scholarships to
V.C.F.de L. and J.E.O. A scientific fishing permit (no. 270295-31003) to collect juvenile lobsters was issued by the Secretary of the
Environment, Natural Resources, and Fisheries (SEMARNAPMe´xico).

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