Journal of Fish Biology (1996) 49, 1102–1111

Food resource partitioning and trophic morphology of

Brevoortia gunteri and B. patronus
M. C-R, A. K  V. Z
Laboratorio de Peces, Departamento de Biologia Universidad Autonoma Metropolitana,
Unidad Iztapalapa, Av. Michoacán y Calzada de la Purísima, Col. Vicentina,
C.P. 09340 México, D.F. Apartado Postal 55-535

(Received 24 November 1995, Accepted 13 May 1996)

The menhadens Brevoortia gunteri and B. patronus are sympatric and morphologically similar.
The two species are planktophagous and exhibited significant (P<0·0001) food resource
partitioning, with phytoplankton predominating in B. patronus stomachs and zooplankton in
B. gunteri. The branchial apparatus of both species is of the typical alosine form. Brevoortia
patronus has significantly more branchiospinules per mm (x̄=19·47) and significantly longer gill
rakers (x̄=13·35 mm) than B. gunteri (x̄=14·11, x̄=12·01 mm respectively). B. patronus is
characterized by a gill raker system forming a fine-meshed filter capable of retaining smaller
food items. The results support the hypothesis that food resource partitioning is related to
different morphological features of the branchial apparatus.
? 1996 The Fisheries Society of the British Isles

Key words: trophic ecology; functional morphology; competition; branchial apparatus;

microphagy; menhaden.

INTRODUCTION
The finescale menhaden Brevoortia gunteri Hildebrand, 1948 and the gulf
menhaden B. patronus Goode, 1879 are similar in body size and external
morphology, and are spatially and temporally sympatric in the Gulf of Mexico,
but B. gunteri is more common in the southern Gulf, whereas B. patronus is more
common in the northern Gulf. Brevoortia gunteri occurs in shallow, coastal
waters from Chandeleur Sound, Louisiana, to Campeche, Mexico, whereas the
geographical range of B. patronus extends from Florida Bay to Campeche,
Mexico (Whitehead, 1985). Both species inhabit estuarine ecosystems, and we
have observed that in Mexico they coexist in five of 13 coastal lagoons in the
Gulf of Mexico.
Many studies have analysed the resource partitioning between fish species
(Ross, 1986), some including B. patronus (Govoni et al., 1983; Chen et al., 1992).
However, none of these studies has examined the resource partitioning between
species of the genus Brevoortia. Morphological differences between species have
often been found to be related to differences in resource use among coexisting
species (Paine et al., 1982). Some studies have used morphological data in an
attempt to explain the differences of the diets among species of fishes (Stoner &
Livingston, 1984). Differences in the morphologies of gill rakers have often been
used for this purpose (Hessen et al., 1988; Pohla & Goldschmid, 1989; MacNeill
& Brandt, 1990).
Tel.: (5) 724 46 94; fax: (5) 724 46 88; email: crma@xanum.uam.mx
1102
0022–1112/96/121102+10 $25.00/0 ? 1996 The Fisheries Society of the British Isles
       1103

Given the morphological similarities and the spatial coexistence of these

species, the food resource partitioning between them and the morphological
differences in the structures related to their feeding were analysed. We also tried
to hypothesize how the food particles are retained and transported from the
branchial apparatus to the oesophagus. The primary goals of our study were:
(1) to describe the interspecific differences between the diets of B. gunteri and
B. patronus; and (2) to describe and analyse the trophic morphology of these
species, particularly the characteristics of the branchial apparatus.

MATERIALS AND METHODS

STUDY AREA
The lagoon of Pueblo Viejo is located in northern Veracruz State, Mexico (22)05*–
22)13* N, 97)50*–98)00* W). It has an area of about 89 km2 and is connected on the
northern side to the Pánuco river, with a slight salinity gradient that increases from
the southern to the northern end. Therefore, we considered two estuarine subsystems,
the marine-influenced habitat (MIH) and the freshwater-influenced habitat (FIH). The
region has a warm and a sub-humid climate with a dry season (December to May) and
a rainy season (July to November).
We used a gillnet to sample fish at five MIH sites and five FIH sites, at 1-month
intervals from August 1987 to September 1990. Immediately after each catch, specimens
were fixed in 10% formalin and later preserved in 70% ethanol. We preserved stomach
contents by injecting 10% formalin directly into the visceral cavity of each fish.

DIET
For the stomach content analyses, we selected approximately the same number of
individuals from each species every month, except in October 1988 and February 1989
when only B. patronus was captured (one and four respectively). A total of 100 specimens
from each species was examined for these analyses, 60 for the rainy season and 40 for the
dry season. We used only adult specimens, since major ontogenetic changes in feeding
habits occur in several species (Livingston, 1982; Ross, 1986). In each case, the stomach
contents were squashed on a graduated slide to a uniform depth and the area of the
squash was measured, according to the method for measuring small stomach volumes
(Hyslop, 1980). We selected a sample (about 20% total area) from the contents of each
stomach, sorted the material, and identified and counted the items in each sample using
a compound microscope (400#). Identification of organisms was made to the lowest
taxon that could be determined consistently with certainty.
The relative importance of each food item to the diet of each species was evaluated
using two methods: (1) the frequency of occurrence of the item (percentage of all
stomachs containing one or more individuals of each food category); and (2) the
numerical percentage of each item (percentage of individuals in each food category of
the total individuals in all food categories), according to Hyslop (1980).
Discriminant analysis was applied to the individual numerical percentages of each
food item as discriminating variables: (1) to determine if the species diets could be
distinguished from one another on the basis of food items; and (2) to identify the most
important food items in differentiating the species diets. We measured directly the
distinctiveness of species diet by means of the Wilks’ ë criterion. The ÷2 test (÷2i) for
the Wilks’ ë was used to test the significance of the overall difference between
species-diet centroids. The relative importance of the original (discriminating) variables
in separating species-diets was gauged by the standardized weights (Tatsuoka, 1988).
This multivariate analysis, as used by Desselle et al. (1978) and Yap (1988), is relatively
superior to the traditional subjective method to discern subtle differences in diets of
fish species.
1104 . -   .

MORPHOLOGY
For each species, six morphological characteristics of the branchial apparatus and gut
structures were examined in 60 specimens. The characteristics of the branchial apparatus
examined were: (1) the number of gill rakers on the inferior limb of the first branchial
arch; (2) the length of the intermediate gill raker (at the junction of the hypo- and
ceratobranchial bones); (3) the number of branchiospinules (per mm) on the intermediate
gill raker; and (4) the length of the epibranchial organs. Counts were made using a
stereoscopic microscope (40#) and lengths were measured with callipers to 0·05 mm
precision.
Particularly, counts of branchiospinules were made under a compound microscope
(400#), with an eyepiece micrometer. The characteristics of gut morphology considered
were: (1) the structure of the stomach; and (2) the length and the coiling pattern of the
intestine. Because the observed variation in the branchial apparatus characteristics and
the length of the intestine is partially attributable to size variation, covariance analysis
(ANCOVA) was used to compare these morphological data. The standard, cephalic and
first gill arch lengths were used as covariates. Additionally, correlation analysis accord-
ing to Sokal & Rohlf (1995) was used to measure the degree of association between the
morphological characteristics and the percent of phytoplankton and zooplankton in each
species.

RESULTS
DIET

The size ranges of the fishes used for the diet and morphological analyses
overlapped considerably (128–177 mm SL for B. gunteri, and 115–162 mm SL
for B. patronus). Mean standard lengths and mean cephalic lengths of B. gunteri
(140·07 mm SL; 44·28 mm CL) and of B. patronus (137·83 mm SL; 43·48 mm
CL) were not significantly different between the two species (P>0·35 for SL;
P>0·25 for CL). The same pattern holds for comparisons within habitats and
within seasons. Brevoortia patronus and B. gunteri are planktophagous, feeding
on various phytoplanktonic and zooplanktonic organisms, such as diatoms,
dinoflagellates, tintinnids, calanoid copepods, and ostracods (Table I). Also,
detritus was a primary food source for both species.
The difference between species diets was statistically significant following the
discriminant analysis (ë=0·5934, ÷2i =47·76, P<0·0001). The most important
food items (based on standardized weights) that contributed to discriminate
between species-diets, were zooplanktonic, namely tintinnids (1·2319), ostracods
(0·8007) and calanoids (0·7111). Therefore, the main interspecific differences
between their diets was the kind of prey. Phytoplankton was the major
constituent of the diet of B. patronus (>72%n of total preys) and was less
represented in the diet of B. gunteri (<49%n of total prey). Conversely,
zooplankton were more common in the diet of B. gunteri (>51%n of total prey)
than in the diet of B. patronus (<28%n of total prey).
This general trophic pattern in which B. patronus consumed more
phytoplankton and B. gunteri preferred zooplankton was repeated in both
habitats (Table II). There were significant differences in diets between species in
MIH (ë=0·3658, ÷2i =28·16, P<0·02) and in FIH (ë=0·5546, ÷2i =31·83,
P<0·005).
Seasonally, B. patronus preferred phytoplankton at all times and B. gunteri
consumed more zooplankton in the rainy season. However, in the dry season
       1105

T I. List of the general food categories, percentage frequency of occurrence (%F) and
numerical percentage (%n) of food items in diet of Brevoortia gunteri and B. patronus

B. gunteri B. patronus
Food items
%F %n %F %n

Phytoplankton 100·00 48·80 100·00 72·40

Centric diatoms 100·00 20·31 100·00 25·38
Navicula 21·05 1·91 38·71 4·57
Nitzchia 23·68 1·68 30·65 1·43
Diploneis 47·37 3·35 62·90 4·24
Other pennate diatoms 10·53 0·80 25·81 1·41
Rhizosolenia 55·26 3·08 77·42 3·64
Other chain-forming diatoms 15·79 1·53 33·87 4·01
Peridiniaceae 65·79 7·38 45·16 9·24
Gymnodiniaceae 57·89 7·23 69·35 17·34
Dinophysiaceae 10·53 1·53 17·74 1·14
Zooplankton 100·00 51·17 91·93 27·51
Tintinida 78·95 28·95 85·48 15·75
Copepoda (Acartia tonsa and
Pseudodiaptomus coronatus) 1·05 14·16 91·93 7·76
Ostracoda 73·68 6·06 65·52 2·86
Cladocera 36·84 2·00 46·77 1·14
Detritus 78·95 87·10

T II. Numerical percentage (%n) of food items in diet of Brevoortia gunteri and
B. patronus by habitat

B. gunteri B. patronus
Freshwater- Marine- Freshwater- Marine–
influenced influenced influenced influenced
habitat (FIH) habitat (MIH) habitat (FIH) habitat (MIH)

Phytoplankton 49·43 47·80 72·53 70·16

Zooplankton 50·57 52·20 27·47 29·84

phytoplankton was the major constituent of its diet (Table III). Discriminant
analyses also showed significant differences in diets between species, during rainy
(ë=0·5340, ÷2i =41·72, P<0·0001) and dry seasons (ë=0·1006, ÷2i =37·89,
P<0·0004).

MORPHOLOGY
The branchial apparatus of B. gunteri and B. patronus is formed by
endochondral bones, which include (as in other clupeids) the following elements:
basibranchials 1–4, hypobranchials 1–3, ceratobranchials 1–5, epibranchials 1–4
and infrapharyngobranchials 1–4 [Fig. 1(a)]. Epibranchial 4 has a laminar
projection that reinforces the epibranchial organ. A mediopharyngobranchial
cartilage is present and tooth-plates were lacking in these species.
1106 . -   .

T III. Numerical percentage (%n) of food items in diet of Brevoortia gunteri and
B. patronus by season

B. gunteri B. patronus
Rainy season Dry season Rainy season Dry season

Phytoplankton 48·21 54·09 69·99 76·86

Zooplankton 51·79 45·91 30·01 23·14

Mediopharyngobranchial
cartilage Epibranchial 4

Cartilaginous
capsule

Infrapharyngobranchial

Ceratobranchials
Gill rakers
Medial wall

Basibranchial 2 10 mm Fifth
Hypobranchials ceratobranchial
(a) (b)

To oesophagus
5 mm

Branchiospinules

Cutaneous
fold

Branchiospinules
0.2 mm
5 mm

(c)

Branchial bone

F. 1. Branchial apparatus of Brevoortia patronus. (a) Osteology of gill arches, lateral view. (b)
Epibranchial organs, frontal section. (c) Gill raker, frontal view. (d) Branchiospinules on the
frontal side of the gill raker.

There are a relatively high number of gill rakers on the hypo-, cerato-, epi-,
and infrapharyngobranchials, most of which are very large [Fig. 2(a)]. The gill
rakers on the infrapharyngobranchials 2–4 are folded. The structures that are
       1107

Mediopharyngobranchial
cartilage
Epibranchial
organs

Liver

Swim bladder

Gill rakers on
first branchial arch
Anus
(a) Pyloric caecae
Intestine
Cardiac stomach

Pneumatic Pneumatic
Blind sac duct duct
Oesophagus

Gizzard
Pyloric stomach 20 mm
Pyloric caecae
(b) (c)

F. 2. Digestive system of Brevoortia patronus. (a) Branchial apparatus and organography of the visceral
cavity, lateral view. (b) Stomach and pyloric caecae, lateral view. (c) Stomach, sagittal section.

important for the retention of food particles are the gill rakers and their
secondary projections [Fig. 1(c), (d)], named branchiospinules by Friedland
(1985). In the internal face of the branchial apparatus there is a set of grooves
built-up by the rakers themselves. Grooves of the inferior limbs of the three first
arches are complemented by cutaneous folds.
Brevoortia patronus has a higher branchiospinule number and, therefore,
these branchiospinules are closer together compared with those of B. gunteri
(Table IV). Epibranchial organs [Fig. 1(b)] are well developed in both species,
but they are longer and have thinner walls in B. patronus than in B. gunteri.
Considering the three covariates, there was no significant difference between
the number of gill rakers (P>0·90), but differences between the number of
branchiospinules (per mm) were significant (P<0·0001). There were also signifi-
cant differences between the lengths of the intermediate gill rakers (P<0·0001)
and between the lengths of the epibranchial organs (P<0·05).
The alimentary tracts of both species have a similar morphology. The
stomach extends posteriorly as a blind sac [Fig. 2(b), (c)]. The pyloric stomach
is partially modified as a gizzard. The intestine is long and has the same pattern
1108 . -   .

T IV. The standard deviations (..) and means (x̄) of the morphological character-
istics of the branchial apparatus of Brevoortia gunteri and B. patronus

Gill raker Intermediate gill Branchiospinules Epibranchial

number raker length (mm) per mm organ length (mm)
x̄ .. x̄ .. x̄ .. x̄ ..

B. gunteri 135·0 4·072 12·01 0·873 14·11 1·830 11·3 0·841

B. patronus 135·2 4·170 13·35 0·781 19·47 2·854 12·0 0·794

of concentric coiling in the two species [Fig. 2(a)]. The intestine of B. patronus
was significantly longer (x̄=553·7 mm) than that of B. gunteri (x̄=451·1 mm),
considering the standard length as covariate (P<0·025).
The correlation between the number of branchiospinules per mm with its
corresponding % of phytoplankton in the diet were significant in B. gunteri
(r=0·70, P<0·05), but not in B. patronus. There were also significant correlations
between the length of the intermediate gill raker with its corresponding percent
of phytoplankton in B. gunteri (r= "0·7, P<0·05), but not in B. patronus.

DISCUSSION
The feeding behaviour of B. patronus is well documented (Chen et al., 1992),
but this information is lacking for B. gunteri. We have found that both species
feed mainly on lagoon organisms and detritus (see also De la Lanza & Cantú,
1986), which includes plankton. The importance of detritus as a food resource
has been reported previously for B. patronus (Deegan et al., 1990).
Our results from discriminant analyses indicate that there are significant
differences in diets between B. gunteri and B. patronus. These differences are
observed in all seasons and habitats analysed. Discriminant analysis served to
identify further major food items that were related (statistically) to changes in
the species diets and to suggest possible functional relationships. The most
important food item discriminating between the species diets was zooplankton
(tintinnids, ostracods and calanoids). Thus, the two species exhibited food
resource partitioning with zooplankton predominating in B. gunteri stomachs
and phytoplankton composing the vast majority of the stomach contents of
B. patronus. Although food partitioning among larvae of B. patronus and other
species has been studied (Govoni et al., 1983; Chen et al., 1992), our data are the
first about food partitioning between two species of Brevoortia.
The differences in morphology, especially in oropharyngeal characteristics,
may lead to a difference in food items ingested (Moyle & Cech, 1996). Some
studies have used mouth features (Hacunda, 1981; Hyslop, 1982; Harnois et al.,
1992), dentition (Goldschmid, 1982; Chen et al., 1992), number of gill rakers
(Lavin & McPhail, 1986; Pohla et al., 1986; Hessen et al., 1988) and morphology
of gill rakers (Pohla & Goldschmid, 1989; MacNeill & Brandt, 1990; Mattson,
1992) to explain the differences of the diets among species of fishes.
The morphological analysis of B. patronus and B. gunteri suggests that the
diet and partitioning of food resources is according to their functional
       1109

morphology. The branchial apparatus of both species corresponds to the

structural organization of the subfamily Alosinae, and that of Brevoortia
tyrannus (La trobe), described by Nelson (1967). The presence of the medio-
pharyngobranchial cartilage allows these menhadens to have more anterior gill
rakers than other clupeiforms. This cartilage and the folds of the gill rakers of
infrapharyngobranchials 2–4, appear to increase the area for filter-feeding
(Miller, 1969).
The most important morphological differences between these species are the
number of branchiospinules and the length of gill rakers. Brevoortia patronus
has more branchiospinules per mm, forming a fine-meshed filter capable of
retaining unicellular algae (generally smaller food items), whereas B. gunteri
filters mainly zooplankton (larger food items). Indeed, the standardized weights
of discriminant analysis indicate that zooplanktonic items were the discriminat-
ing variables in species diets. The relation between the characteristics of
branchial apparatus (number of branchiospinules and gill raker length) and the
percent of ingested phytoplankton was confirmed by correlation analyses, which
were significant for B. gunteri. The correlations in B. patronus were not
significant, probably because this species has a finer mesh network, which
enables it to select both small and large food items. Thus, evidence indicates that
interspecific differences between the diets of B. patronus and B. gunteri are
correlated with the morphological differences between their branchial apparatus.
Werner (1979), Hacunda (1981), Lavin & McPhail (1986), and Santamarina
(1993) have shown that the prey size plays an important role in trophic
partitioning. Particularly in clupeids, trophic partitioning by food size was
studied by Davies & Foltz (1991), where the herring Alosa aestivalis (Mitchill)
fed on larger prey and the gizzard shad Dorosoma petenense (Günther) fed on
smaller prey, mainly phytoplankton.
According to the structure of the branchial apparatus of B. gunteri and
B. patronus, probably the food particles captured by the branchiospinules
descend to the base of the raker. They are transported backwards through the
grooves reaching the confluence of the superior and inferior limbs of each
branchial arch. From this point, particles are transmitted to the second and
subsequent arches reaching a groove between the fourth and fifth arches. From
here, they are carried to the epibranchial organs, and then to the oesophagus.
A similar mechanism of transport was proposed by Friedland (1985) for
B. tyrannus.
As in other clupeoids, the epibranchial organs concentrate and store food
particles temporarily. Their relationship to other branchial features or to
alimentary structures has not been reported previously. We find that in these
species of Brevoortia, longer epibranchial organs correspond to longer gill rakers,
greater numbers of branchiospinules, and longer intestines. The partial modifi-
cation of the pyloric stomach as a gizzard and the presence of a blind sac in the
stomach also suggests a microphagous feeding habit for these menhaden species.
The intestinal lengths of B. gunteri and B. patronus may be related to their
respective type and size of prey, since gut lengths are often greater in those fish
that feed on detritus, algae and small organisms than those that feed on large
organisms (Chao & Musick, 1977; Moyle & Cech, 1996). Thus, B. patronus has
a longer intestine and consumes more detritus and algae than B. gunteri.
1110 . -   .

Our results suggest that resource partitioning between these two species is due
mainly to differences in branchial apparatus morphology and it could facilitate
their local coexistence.

We thank J. Schmitter, A. Zavala and three anonymous reviewers for their helpful
reviews of this paper and comments on the manuscript; and the Secretaría de Educación
Pública and the Universidad Autónoma Metropolitana for their support of this
research.

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