Feeding ecology of the three juvenile phases of the spiny lobsterPanulirus argus in a tropical reef lagoon Received: 26 January 2002 / Accepted: 9 December 2002 / Published online: 12 Fe
Trang 1Feeding 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
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
ju-venile 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
abun-dance of the larger juveniles Juveniles were collected
by divers at night, from January to November 1995,
throughout the mid-lagoon and back-reef zones
Per-cent 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
be-cause postmolt individuals had emptier stomachs The
main food categories in all juvenile phases were
crus-taceans (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
vegetation The most abundant taxa in all sites were decapods and gastropods, but density and diversity measures showed that the distribution of these poten-tial 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 pro-tracted 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 cara-pace 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 re-main 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.
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
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: briones@mar.icmyl.unam.mx
Fax: +52-998-8710138
Trang 2P 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 (2051¢N; 8653¢W; Fig 1a) are among the
latter (Padilla-Ramos and Briones-Fourza´n 1997),
de-spite high indices of postlarval influx into the Puerto
Morelos reef lagoon (Briones-Fourza´n 1994) To
inves-tigate the possible causes for this paradox, the
popula-tion 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
indi-viduals 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
(Briones-Fourza´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
Loz-ano-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
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 Briones-Fourza´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 sim-ilar 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 5–6C (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) ex-tends 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
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
856
Trang 3mostly 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,
domi-nated 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
Lozano-A´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 24.50C in the winter
(January–February), 27.22C in the spring (March–May), 29.41C
in the summer (June–August), and 28.54C 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
col-lected 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
col-lected 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)4C 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
poste-rior 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
dis-sected 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
indi-viduals 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
dif-ferences 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 stom-achs 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 rela-tive contribution to the diet of food items of different sizes Sta-tistical 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 stan-dardizes 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 back-reef 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 indi-viduals were collected in the mid-lagoon Therefore, we excluded sex and sampling zone from the factorial analysis and ran inde-pendent Student’s t-tests on each of them We then ran a three-factor 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 in-traspecific groups, index values £ 0.8 are considered to be indi-cative 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 com-parisons (Drazen et al 2001)
857
Trang 4Study 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
epi-benthic 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
com-posed of slow-moving, epibenthic macrofauna, particularly
deca-pod and gastrodeca-pod 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 was342 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
as-semblages 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
loga-rithms 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
juve-niles 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
esti-mated in 176 individuals As expected, there were no
effects on the RWDG of either sex (mean±SE of
fe-males: 4.11±0.10; of fe-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 consis-tently lower in subadults.
The most distinct components of the stomach con-tents of juvenile P argus in all four seasons were crus-taceans (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 gastro-pod 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, forami-nifers, and remains of tunicates, bryozoans, and corals Plant food categories comprised pieces of seagrass blades and macroalgae, as well as coralline algae Al-though 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 di-gested 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 stom-achs 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
(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 coeffi-cients were significant, and all the values of Horn’s index
858
Trang 5were >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
sea-sonal changes in the relative volumetric composition of
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 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)
Molt stage Intermolt 72 4.30±0.13
Premolt 86 4.35±0.10 Season Winter 47 4.12±0.17
Spring 49 4.31±0.16 Summer 36 4.42±0.10 Autumn 45 4.33±0.13 Juvenile phase Algal 46 4.49±0.16
Postalgal 91 4.39±0.11 Subadult 40 3.80±0.11
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 barsrepresent
sample sizes
Table 2 Juvenile Panulirus argus Results of the three-factor ANOVA (fixed factors) on log-transformed data (see Table 1) Effect df Mean square F-value P A: Molt stage 1 0.274 0.315 0.575 B: Season 3 0.084 0.097 0.962 C: Juvenile phase 2 4.249 4.906 0.009 A·B 3 0.669 0.772 0.512 A·C 2 0.319 0.369 0.692 B·C 6 0.465 0.537 0.780 A·B·C 6 0.536 0.618 0.715 Error 135 0.866
859
Trang 6included species of fishes, polychaetes, echinoderms,
sponges, and other taxa Decapod crustaceans and
gas-tropod 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
la-goon (the most abundant species following in
paren-theses) were caridean shrimps of the families
Hippolytidae (Latreutes fucorum, Thor manningi) and
Palaemonidae (Periclimenes americanus), followed by
hermit crabs of the families Paguridae (Pagurus
annuli-pes, P brevidactylus) and Diogenidae (Clibanarius
tri-color) 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
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 Briones-Fourza´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
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
Factor Pairwise comparison Horn’s overlap index Spearman’s correlation coefficient Sex Females vs males 0.973 (+) 0.952***
Juvenile phase Algal vs postalgal 0.978 (+) 0.917**
Postalgal vs subadult 0.969 (+) 0.830**
Algal vs subadult 0.950 (+) 0.900**
Molt stage Postmolt vs intermolt 0.907 (+) 0.768*
Intermolt vs premolt 0.986 (+) 0.935**
Premolt vs postmolt 0.918 (+) 0.775**
Season Winter vs spring 0.930 (+) 0.971***
Spring vs summer 0.942 (+) 0.875**
Summer vs autumn 0.928 (+) 0.945***
Autumn vs winter 0.814 (+) 0.708n.s
Spring vs autumn 0.876 (+) 0.634*
Winter vs summer 0.903 (+) 0.893**
Sampling zone Mid-lagoon vs back-reef 0.945 (+) 0.618**
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
Food categories Winter (34) Spring (41) Summer (37) Autumn (39)
Crustaceans 88.2 30.4 92.7 43.4 91.9 34.4 94.9 36.8 Gastropods 88.2 14.5 92.7 19.4 89.2 22.1 94.9 16.4 Plant matter 70.6 4.4 48.8 2.7 67.6 4.5 53.8 1.8 Sediment 70.6 11.9 61.0 3.7 70.3 7.3 97.4 6.0 Soft matter 82.4 14.8 82.9 15.0 97.3 24.2 100.0 15.5 Sponges 47.1 16.5 48.8 7.9 16.2 2.4 12.8 0.8 Bivalves 38.2 2.7 41.5 3.8 2.7 0.2 12.8 1.0 Calcareous algae 14.7 0.9 14.6 0.2 8.1 0.1 18.0 0.2 Echinoderms 2.9 0.4 2.4 0.1 5.4 1.4 46.1 13.0 Foraminifers 41.2 0.8 39.0 0.3 40.5 0.5 64.1 0.6
Barnacle postlarvae 2.9 0.2 9.8 1.4 5.4 0.1 0 0 Polychaetes 0 0 17.1 1.1 21.6 1.8 41.0 4.3
Chitons 0 0 4.9 0.5 8.1 0.4 35.9 3.4
860
Trang 7large 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
domi-nance indices.
Discussion The diet of juvenile Panulirus argus included a wide food spectrum, similar to the diet of adult P argus
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 parenthesesare
number of species identified in
each taxon Asterisks denote
those taxa that were represented
in stomach contents of juvenile
Panulirus argus
Taxon Density (individuals ha)1) per site Average
Site 1 Site 2 Site 3 Site 4 Site 5 Crustacea (79) 190,146 130,263 285,789 112,953 68,742 157,579 Stomatopoda (2)* 556 614 702 0 439 462 Amphipoda (2)* 88 58 117 205 292 152 Isopoda (8)* 1,082 1,404 1,462 146 906 1,000 Penaeidae (1) 322 673 731 88 88 380 Sicyoniidae (2) 468 702 1,082 760 1,930 988 Palaemonidae (3) 40,994 39,942 55,000 6,374 4,386 29,339 Alpheidae (4)* 8,450 5,643 10,146 0 2,544 5,357 Hippolytidae (7) 70,819 67,018 137,339 38,450 32,193 69,164 Processidae (3) 4,152 8,012 9,094 3,041 8,538 6,567 Palinuridae (1) 263 117 146 29 175 146 Diogenidae (9)* 7,573 205 3,626 4,942 175 3,304 Paguridae (4)* 51,433 4,942 62,076 56,228 14,532 37,842 Majidae (16)* 2,193 468 2,661 2,339 1,988 1,930 Portunidae (2)* 1,053 351 1,053 351 292 620 Xanthidae (11)* 673 117 378 0 117 257 Other decapods (4)* 29 0 175 0 146 70 Mollusca (48) 119,268 43,129 87,105 106,404 66,024 84,386 Trochidae (3)* 23,421 5,965 10,439 526 1,959 8,462 Turbinidae (2) 8,246 3,129 2,982 614 497 3,094 Phasianellidae (1)* 21,813 14,708 43,830 70,906 43,246 38,901 Neritidae (1)* 2,368 994 1,433 2,632 234 1,532 Modulidae (1)* 10,029 6,784 8,187 789 3,187 5,795 Cerithiidae (2)* 47,310 10,526 13,216 6,082 3,801 16,187 Crepidulidae (2) 234 58 205 0 205 140 Epitoniidae (1) 409 0 234 673 175 298 Columbellidae (1)* 673 234 1,901 15,731 7,982 5,304 Nassariidae (1) 1,140 88 2,924 6,082 994 2,246 Other gastropods (21)* 2,544 556 1,579 2,339 3,187 2,181 Bivalvia (8)* 731 88 146 29 351 269 Other molluscs (4)* 350 0 29 0 205 117 Other taxa (46) 7,894 4,123 5,585 2,309 1,316 4,246 Polychaeta (6)* 88 0 117 0 468 135 Echinodermata (6)* 205 0 205 58 468 187
Pisces (25)* 7,544 4,123 5,234 994 146 3,608
Total taxa (173) 317,308 177,515 378,479 221,666 136,082 246,211
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 variegatais grams of
dry weight per square meter
Assemblage Characteristics Sampling site
Crustaceans Species richness (S) 51 37 62 36 53
Number of individuals (N) 6,512 4,455 9,775 3,864 2,351 Diversity (HD) 9.545 7.434 9.934 6.246 12.158 Evenness (J¢) )1.676 )4.605 )1.831 )1.752 )1.472 Dominance (d) 0.236 0.314 0.196 0.344 0.283 Mollusks Species richness (S) 32 19 28 24 25
Number of individuals (N) 4,079 1,487 2,978 3,639 2,253 Diversity (HD) 8.281 7.036 6.178 3.387 4.154 Evenness (J¢) )1.352 )0.993 )1.511 )1.958 )1.795 Dominance (d) 0.201 0.338 0.503 0.666 0.656 Vegetation Seagrass density 639.2 560.0 507.2 0 198.4
Macroalgal density 72.0 211.8 107.6 103.2 109.4 Biomass of L variegata 25.0 24.7 5.0 0 0
861
Trang 8(Herrnkind et al 1975; Colinas-Sa´nchez and
Briones-Fourza´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
feed-ing 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
con-trast, 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
stom-achs, 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
palinur-ids, 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
juve-niles seek shelter, are scarce and overdispersed
throughout the lagoon (Briones-Fourza´n and
Lozano-A´lvarez 2001b) The back-reef zone is richer in den
re-sources 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;
Stu-dent’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 Briones-Fourza´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 fre-quent 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 distri-bution 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 crus-tacean taxa (caridean shrimps) were altogether absent in their guts (see Table 5) As is the general case in palin-urids (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 be-longed 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 fast-moving animals, probably belonged to dead or injured individuals Our juveniles also consumed infaunal spe-cies, such as small bivalves, polychaetes, and foramini-fers, 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
862
Trang 9requires greater energy than the capturing of
slow-moving 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
im-portant component of the diet (Joll and Phillips 1984;
Edgar 1990).
We only sampled the epifauna during summer,
be-cause 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
dif-ferences 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
uncom-mon food sources when the abundance of the latter
in-creases 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
(mus-sels) 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)
Never-theless, the high diet overlap among seasons indicate
that, despite possible seasonal differences in prey
avail-ability, 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
nu-tritional 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
re-duced the availability of food in the winter
(Lozano-A´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 nutri-tional condition than their smaller counterparts, irre-spective 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 in-crease 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 anal-ysis Thus, the reasons for the poorer nutritional con-dition 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 alter-native explanation invokes the scarcity of crevice-type shelters suitable for subadults throughout the reef la-goon (Briones-Fourza´n and Lozano-A´lvarez 2001b) The lack of shelter resources increases predation-in-duced mortality (Smith and Herrnkind 1992) and may thus restrict the foraging movements of subadults to minimize their risk of predation, precluding their ex-ploitation of food resources in areas where shelter is limited, or it may affect their foraging efficiency by in-creasing 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 seem-ingly poor nutritional condition of subadults, in conjunction with the lack of appropriate natural shelters for this benthic stage (Briones-Fourza´n and Lozano-A´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 Monroy-Vela´zquez, E Cadena-Barrientos, F Solı´s, and F Escobar de la Llata helped to identify the epifauna F Ruiz-Renterı´a kindly
863
Trang 10provided the water temperature data Comments by three
anony-mous 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
270295-310-03) to collect juvenile lobsters was issued by the Secretary of the
Environment, Natural Resources, and Fisheries
(SEMARNAP-Me´xico)
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