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BULLETIN OF MARINE SCIENCE, 66(2): 361–373, 2000
TROPHIC INTERRELATIONS OF THE THREE MOST ABUNDANT
FISH SPECIES FROM LAGUNA SAN IGNACIO,
BAJA CALIFORNIA SUR, MEXICO
V. H. Cruz-Escalona, L. A. Abitia-Cardenas,
L. Campos-Dávila and F. Galvan-Magaña
ABSTRACT
We analyzed the trophic interrelations of cominate sea catfish Arius platypogon, shortfin
weakfish Cynoscion parvipinnis, and California king croaker Menticirrhus undulatus
from Laguna San Ignacio, B.C.S., Mexico during spring and summer 1992. Four different trophic groups were found on the basis of feeding preferences; crustaceans, fish,
mollusks, and polychaetes. Each predator species has a preference for specific prey. For
A. platypogon, the dominant prey was Callinectes bellicosus; for C. parvipinnis, the species Penaeus californiensis and Ophistonema libertate were the main prey; and for M.
undulatus, the dominant preys were P. californiensis and Donax sp. The food habits of
these predator species have some seasonal and spatial changes, however according to the
Morisita-Horn index no significant trophic overlap exists. The results of this study show
the coexistence of these predator species are a function of a spatial segregation and the
distribution of available food resources in the lagoon.
Knowledge of the ichthyofauna of the coastal systems is one of the most importance
aspects in biology and ecology studies needed to evaluate the biotic resources of a given
area (Mayard et al., 1982). The coastal lagoons have been recognized as important zones
for the nourishment, nursing, and reproduction of many fish species (Ribeiro et al., 1997)
because of their large number of different habitats, great food resources, and low incidence of predators (Day and Yañez ,1985; Vega, 1998).
Much of the prey consumed by predatory fish are species with commercial importance. Among such species are crustaceans, which include the commercially important
shrimp and crab (Sibert, 1981; Divita et al., 1983; Minello and Zimmerman, 1984; Minello
et al., 1987; Day et al., 1989).
Ecological studies, in particular those directed to the knowledge of trophic ecology
(types of prey consumed, diet breadth, and relative importance of each nutritional component), are useful to understand the functional role of the fish within these ecosystems
(Zaret and Rand, 1971; Wootton, 1990). The quantification of the trophic overlap of coexistent species is important to establish the structure of the trophic chain in the coastal
ecosystems and the availability of food resources in the coastal lagoon assemblages
(Caragistou and Papaconstantinou, 1993).
Laguna San Ignacio is part of an ecological reserve named “La Reserva de la Biosfera
de El Vizcaino” because of the importance of the lagoon as a breeding and nursery area of
migratory birds and the gray whale Eschrichtius robustus. Despite its ecological importance, little biological information on the fish species inhabiting the lagoon exists
(Danemann and De la Cruz, 1993; Villavicencio and Abitia, 1994; Segura et al., 1997 and
De la Cruz and Cota, 1998).
The present paper describes the diet of three of the most abundant species of fish collected with a gill net in this area, the cominate sea catfish Arius platypogon, shortfin
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weakfish Cynoscion parvinnis, and California king croaker Menticirrhus undulatus, including data on interspecies diet overlap and diet breadth to provide new and basic knowledge of their trophic ecology.
STUDY AREA
Laguna San Ignacio is on the west coast of the Baja California Peninsula, Mexico, between
26°38' and 27°00'N and 113°06' and 113°18'W (Fig. 1). It has an approximate area of 17,500 ha,
and is almost 6 km long and 6 km wide (Contreras, 1985). It is a shallow lagoon of temperate
affinity with depths of 2 to 4 m in the deep area, and 20 m in the channels, which connect to the
Pacific Ocean (Swartz and Cummings, 1978).
The lagoon has sandy beaches, muddy lowlands, patches of rocky coast, and mangrove zones of
Rhizophora mangle (Swartz and Cummings, 1978). Jones and Swartz (1984) divided the lagoon
into three areas: (1) Lower Lagoon; the entry that links the lagoon with the sea. In this zone are
found channels approximately 10 and 20 m deep near the entry, (2) Central Lagoon; extends from
the lower lagoon. In this section are found three channels separated by two large sand banks, (3)
Upper Lagoon; the inner area of the lagoon, mostly shallow, with two exposed zones (Fig. 1).
METHODS
The fish were collected in two samplings (May and August 1992) with a gill net 140 m long, 3 m
wide, and a mesh size of 9 cm. The nets were set in the three areas of the lagoon, delimited by Jones
and Swartz (1984), with the same sampling effort. The nets were set at sunset (18:00) and recovered
at sunrise (06:00). To reduce the digestive processes, the organisms were injected with a solution of
10% formaldehyde neutralized with sodium borate into the abdominal cavity. In the laboratory, the
fish were dissected and the stomachs removed.
In the gastric content analyses, the different prey species were separated by their taxonomic
group, and identified to the lowest possible taxon permitted by the degree of digestion.
The prey were recorded quantitatively, by number (N), weight (W) in grams, and frequency of
occurrence (FO) (Hyslop, 1980). The Index of Relative Importance (IRI) of Pinkas et al. (1971)
was also used to corroborate the importance of each feeding component.
IRI = (W + N ) FO
where IRI = index of relative importance, W = percent weight, N = percent number, and FO =
percent frequency of occurrence. This index frequently has been used in feeding studies because it
has the capacity of showing food components of great importance within the trophic spectrum
(Hyslop, 1980; Segura et al., 1997). This index is expressed as a percentage, with higher values
indicating greater importance.
To describe the spatial and temporal variation in the diversity of the trophic spectrum, the diversity index of Shannon-Wiener (Vandermeer, 1981) was used.
H' = −
s
∑ Pj ln Pj
i =1
where H´ = Shannon-Wiener index, S = total number of identified prey species, and Pj = Number of
the i species, expressed as its proportion of the sum of Pj for all the prey species.
Also the evenness index of Pielou (Krebs, 1989) was calculated using the following equation:
E=
H'
MH '
CRUZ-ESCALONA ET AL.: TROPHIC INTERRELATIONS OF FISHES
363
Figure 1. Study area; where a: lower lagoon; b: central lagoon and c:upper lagoon.
where E = evenness index; H´= Shannon-Wiener index and MH' = maximum possible diversity.
Diet breadth was calculated using Levin’s standardized index (Krebs, 1989) according to the
methodology followed by Labropoulou and Eleftheriou (1997):
Bi = 1 / n − 1{(1 /
∑ jPij 2 ) − 1}
where Bi = Levin’s index for the predator i, Pij = proportion of the diet of predator i that is made up
of prey j, and n = the number of prey categories.
This index ranges from 0 to 1; low values (<0.6) indicate a diet dominated by few prey items
(specialist predator) and higher values (>0.6) indicate generalist diets (Krebs, 1989; Labropoulou
and Eleftheriou, 1997).
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Table 1. Summary of food components in stomach of predator species Arius platypogon,
Cynoscion parvipinnis, and Menticirrhus undulatus from Laguna San Ignacio; expressed as
percentage of index of relative importance (IRI).
Arius platypogon
Prey
Crustacea
Callinectes bellicosus
Portunus xanthusii
Portunidae remains
Hepatella amica
Dynomene ursula
Majidae
Penaeus californiensis
Solenocera sp.
Scycionia sp.
Squilla sp.
Paracerseis sp.
Cirolana sp.
Mysidacea
Hyale sp.
Corophium sp.
Ostracoda
Mollusca
Octopus sp.
Nasarius sp.
Anachis sp.
Ensis californiensis
Tagelus sp.
Donax sp.
Laevicardium sp.
Mollusk remains
Anelida
Lumbrineris sp.
Polychaeta
Echinodermata
Holoturiidae
Osteichtyes
Sardinops caeruleus
Opisthonema libertate
Syngnathus californiensis
Paralabrax maculatofasciatus
Blennidae
Fish remains
Stomach analized
% Stomach contained food
% IRI
Cynoscion
parvipinnis
% IRI
59.74
2.62
2.27
0.02
0.02
9.85
0.34
23.19
3.32
45.69
0.95
Menticirrhus
undulatus
% IRI
0.26
48.30
0.01
4.38
1.62
0.01
0.61
1.04
0.02
11.06
0.06
0.88
0.97
0.11
0.09
0.61
9.31
27.26
1.19
0.51
0.20
0.14
2.64
5.26
0.70
1.38
0.28
0.17
0.03
0.17
102.00
91.10
0.78
24.24
11.10
41.00
100.00
31.00
100.00
CRUZ-ESCALONA ET AL.: TROPHIC INTERRELATIONS OF FISHES
365
The interspecies dietary overlap was estimated using the Morisita-Horn Index (Horn, 1966; Smith
and Zaret, 1982):
Cλ = 2
n
∑
( Pxi × Pyi ) / ( Pxi +
i =1
n
∑ Pyi 2 )
i =1
where Cλ = Morisita-Horn Index of overlap between predator x and predator y, Pxi = proportion
prey i of the total prey used by the predator x; Pyi = proportion prey i of the total prey used by the
predator y, and n = total number of prey. Cλ values vary from 0, when no elements of the diet are
alike, to 1 when all elements occur in equal abundance. The trophic overlap was classified according to the scale proposed by Langton (1982); low overlap 0.0 to 0.29, middle overlap 0.30 to 0.65,
and high overlap 0.66 to 1.
RESULTS
DIET COMPOSITION.—A total of 174 stomachs (A. platypogon = 102, C. parvippinis =
41, and M. undulatus = 31) were analyzed in this study. Of the stomachs sampled, 95%
had identifiable food. A total of 33 prey were identified in five major taxonomic trophic
groups: crustaceans, mollusks, polychaetes, echinoderms, and fish (Table 1). In table 1 is
presented the sample size by species , lagoon area and season.
From the index of relative importance (IRI), the prey warrior swimcrab Callinectes
bellicosus and the yellowleg shrimp Penaeus californiensis provided 95% of the total
importance within the trophic spectrum of A. platypogon (Table 1).
For the food preferences of C. parvipinnis, we observed crustaceans and fish were the
groups with highest contribution. The yellowleg shrimp and the Pacific thread herring
Opisthonema libertate were considered as preferential components (Table 1).
For M. undulatus, the most important prey, using the values of IRI, were crustaceans
and mollusks. The preferential prey was The yellowleg shrimp and the bivalve Donax sp.
(Table 1).
SEASONAL AND SPATIAL VARIATION.—The food habits of the three predator species had
some changes in the composition of their seasonal and spatial diets. Figure 2 shows during spring and summer A. platypogon maintains its preference for warrior swimcrab and
the yellowleg shrimp. The diet of A. platypogon appears to be similar in all zones of the
lagoon (Fig. 2), through some of the prey considered as secondary were important in the
trophic spectrum of this predator in some zones of the lagoon.
For C. parvippinis, a behavior different from A. platypogon was observed because here
we recorded some changes in seasonal prey composition. Figure 3 shows that during
spring this predator consumed the yellowleg shrimp, whereas during summer the Pacific
thread herring was the main prey. For spatial composition, there were few important
changes, except in the central zone of the lagoon during the summer when the diet mainly
was made of secondary prey (Fig. 3).
M. undulatus was the species with most changes in food habits. During spring, the
major source of food was mollusks (Donax sp. and Tagelus sp.), whereas in summer,
there was a greater incidence of crustaceans, mainly the yellowleg shrimp (Fig. 4). The
spatial variation in the food components showed important changes in all the lagoon’s
zones. This variation was greatest in spring, whereas in summer a low variation was found
(Fig. 4).
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Figure 2. Seasonal and spatial variation of the major prey species in the diet of Arius platypogon,
determined by index of relative importance (IRI).
CRUZ-ESCALONA ET AL.: TROPHIC INTERRELATIONS OF FISHES
367
Figure 3. Seasonal and spatial variation of the major prey species in the diet of Cynoscion parvippinis,
determined by index of relative importance (IRI).
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DIET BREADTH AND TROPHIC OVERLAP.—The trophic diversity of the diet of the three
predator species is relatively low, ranging between 0.2 and 1.6 beles / ind. The results
agree with the low values of evenness (0.14–0.65), and Levin’s standardized index values
(0.03–0.25) for each of the three species (Table 2). The results of the trophic behavior of
the three predators indicate they are specialist fish.
According to the Morisita-Horn index, and criteria proposed by Langton (1982), no
significant trophic overlap exists (l > 65%). In spring the interaction A. platypogon - C.
parvippinnis had the highest value of all the possible combinations (l = 0.64), which is the
lower limit of the significant overlap. The rest of the interactions were always at lower
levels (l < 0.3).
DISCUSSION
Though some studies on the food habits of coastal fish have been done in Mexico (e.g.,
Abitia et al., 1990; Segura et al., 1997; Vega, 1998), few have been concerned with analyzing the interactions among the coexisting species. This knowledge is necessary to understand the dynamics of the ecological relations that exist between species and consequently provides information that contributes to the management of the fishing resources
(Day and Yañez, 1985; Caragistou and Papaconstantinou, 1993).
The analysis of the stomach contents showed that the relative importance of a particular food component changed among the predators analyzed. A. platypogon in though consuming a large number of species, selects a reduced number of prey from the benthic
environment (more than 90% originate from this habitat). Evidence of the high degree of
food specialization of this species, is the large consumption of the crustaceans warrior
swimcrab and the yellowleg shrimp.
Several authors have indicated that fish are important regulators of the structure of
benthic communities. Minello and Zimmerman (1984) mentioned that many species of
fish strongly impact some populations of crustaceans, some of which have commercial
importance. The particular high incidence of the crustaceans warrior swimcrab and the
yellowleg shrimp within the stomach of A. platypogon in Laguna San Ignacio may indicate this predator affects the recruitment periods and abundance of these prey species of
high commercial value in the zone.
The food habits of C. parvippinis, feed on crustaceans, polychaets, and mollusks from
the soft bottoms. This indicates this predator is associated with this habitat. This species
also feeds on pelagic prey (California pilchard and Pacific thread herring), which are an
important proportion of their diet.
C. parvippinis is a specialist predator because feed on particular prey (e.g., yellowleg
shrimp, warrior swimcrab and Pacific thread herring). The prey selectivity shown by this
predator is a function of prey size, morphology, taste, and the availability of prey in the
environment (Main, 1985). Also is important to consider the morphological characteristics of the predator (e.g., mouth, teeth, sensory structures) used to capture prey (Chao and
Musick, 1977).
Minello and Zimmeman (1984) and Minello et al. (1987) found similar results in other
sciaenid species (C. nebulosus) from Galveston Bay, U.S.A. They found the food spectra
included mainly shrimp (Penaeus aztecus) and fish, but with preference of shrimp. This
CRUZ-ESCALONA ET AL.: TROPHIC INTERRELATIONS OF FISHES
369
Figure 4. Seasonal and spatial variation of the major prey species in the diet of Menticirrhus undulatus,
determined by index of relative importance (IRI).
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Table 2. Seasonal comparisons of the ecological attributes of the diet of Arius platypogon,
Cynoscion parvipinnis and Menticirrhus undulatus from Laguna San Ignacio.
Ecological attributes
Arius platypogon
Richness
Diversity index
Eveness
Diet breadth
Cynoscion parvipinnis
Richness
Diversity index
Eveness
Diet breadth
Menticirrhus undulatus
Richness
Diversity index
Eveness
Diet breadth
Spring
Summer
13
1.83
0.71
0.17
23
1.83
0.59
0.03
9
1.87
0.85
0.25
5
0.90856
0.56452
0.15
8
1.44
0.69
0.02
4
1.006
0.72
0.17
conclusion came from prey selection in laboratory experiments. They also mentioned
that sciaenids are the main predators of shrimp in coastal lagoons .
The other species analyzed, M. undulatus also included prey from the benthic environment. The dominance of some prey indicated that this predator does a prey selection (e.g.,
Donax spp. and yellowleg shrimp). The feeding behavior of this species is related mainly
to the sensory structures below the mouth, which permit them to locate prey in soft bottoms.
In other coastal lagoons, the sciaenids feed mainly on crustaceans, mollusks, and
polychaets in lower percentages (Chao and Musick, 1977; DeLancey, 1989; Chao, 1995;
Amezcua, 1996; Bocanegra, 1998). Our results were similar to the information reported
by these authors.
There is a dependency of many species on coastal environments, because physical processes (e.g., upwelling, currents) and biological processes (e.g., recruitment), determine
the availability of food resources. Considering these factors, the changes observed in the
trophic preferences of each predator analyzed can explain our results. This trophic variation can be related to morphologic changes in the mouth and locomotive capacity (Chao
and Musick, 1977), energetic requirements as a function of their physiological changes
(e.g., reproduction, growth) and the trophic behavior of each predator species (Gerking,
1994).
Wootton (1990), in addition to the factors mentioned, indicates the changes with age in
the use of the habitat, are other important factors in the food preference variation of each
fish, because the age implies a partitioning of food or habitat between two or more species or between several classes of the same species to exploit the food resources efficiently.
All these elements can explain the coexistence of these predator species in Laguna San
Ignacio. Ross (1986) defines partitioning resources as any use by the species that coexist,
including the food and the habitat. All these elements help keep a low overlap between
predator species. Farnsworth and Ellison (1996) indicated that the diet overlap measure
CRUZ-ESCALONA ET AL.: TROPHIC INTERRELATIONS OF FISHES
371
serves to compare the use of food resources between the species that coexist in a given
community, arguing that such measures serve to define some distribution patterns between the community components.
In conclusion, crustaceans constitute the most important prey in the food preferences
of the three species analyzed. Vega (1998) indicates the importance of crustaceans as
food of fish in coastal systems is because of the great availability of this resource. This
implies that regardless of the energetic value of the prey consumed, their abundance can
considerably reduce the time that the predator needs to hunt and consequently increases
the energetic consumption per unit time. Within the benthic crustaceans, the high selection toward yellowleg shrimp and warrior swimcrab is probably caused by the proximity
to the bottom sediments in comparison with infaunal species such as polychaetes, mollusks, cumacea, and isopods.
Our results coincide with that reported by several authors (Divita et al., 1983; Minello
and Zimmerman, 1984; Minello et al., 1987), who noted that several fish species of the
coastal zone (coastal lagoons, tidelands, estuaries, and marshes) feed on several prey
species of crustaceans and fish that inhabit these places for the purpose of nursing, nourishment, and protection.
ACKNOWLEDGMENTS
The institutional and financial support for this study was provided by the Instituto Politecnico
Nacional (PIFI and COFAA) and Consejo Nacional de Ciencia y Tecnología. Our thanks to U.
Markaida (CICESE) and an anonymous reviewer for their comments, and E. Glazier (CIBNOR) for
editing the English-language text.
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DATE SUBMITTED: April 30, 1999.
DATE ACCEPTED: October 22, 1999.
ADDRESSES: (V.H.C.-E., L.A.A.-C., F.G.-M.) Centro Interdisciplinario de Ciencias Marinas-IPN,
Apartado postal 592, La Paz, B.C.S., Mexico, C.P. 23000. (L.C.-D.) Centro de Investigaciones
Biológicas del Noroeste, S.C., Mexico. CORRESPONDING AUTHOR: (V.H.C.-E.) Centro Interdisciplinario
de Ciencias Marinas, Apdo. Postal 592, 23000, La Paz, B. C. S., Mexico; Tel.: (112) 2 53 44; fax::
(112) 2 53 22; Email <[email protected]>.