Journal of Fish Biology (2006) 68, 1782–1794
doi:10.1111/j.1095-8649.2006.01061.x, available online at http://www.blackwell-synergy.com
Determination of feeding mode in fishes: the importance
of using structural and functional feeding studies in
conjunction with gut analysis in a selective
zooplanktivore Chirostoma estor estor Jordan 1880
L. G. R OSS *†, C. A. M ARTÍNEZ -P ALACIOS ‡,
Ma. del C. A GUILAR V ALDEZ ‡, M. C. M. B EVERIDGE §
Ma. C. C HAVEZ S ANCHEZ k
AND
*Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, U.K.,
‡Coordinación de la Investigación Cientı´fica, Ciudad Universitaria, Universidad
Michoacana de San Nicolás de Hidalgo, Michoacán, Morelia, Me´xico, §Fisheries
Research Services, Freshwater Laboratory, Faskally, Pitlochry, PH16 5LB, Scotland,
U.K. and kUnidad Mazatlán en Acuicultura y Manejo Ambiental del CIAD, A.C. Av.
Sábalo Cerritos s/n, Apdo Postal 711. Mazatlán, CP. 82010, Sinaloa, Me´xico
(Received 31 May 2005, Accepted 21 December 2005)
Anatomical and histological studies of the endangered atherinid Chirostoma estor estor reveal
that the species is ideally adapted to feeding on zooplankton. It has a superior protractile
mouth with short unicuspid mandibular teeth. The buccal cavity is a highly adapted branchial
sieve with branchial spines which develop in complexity with age to form a continuous flexible
interdigitated mat. The filter bed has many of the characteristics of a cross-flow filter, which is
ideal for a continuously feeding and filtering animal as the filter bed will not readily become
occluded. The aggregates from the cross-flow filter pass to the rear of the buccal cavity where
they are triturated by well-developed pharyngeal teeth. The species has a short intestine (<03 body length) with no histological evidence of stomach-like structures, no pyloric caecae and
with trypsin-like enzymes operating at high pH. Feeding trials with natural plankton showed
a sequence of particle size selection as the animals grow, with older animals taking
cladocerans up to 700 mm in diameter. Although some adults occasionally take small fish prey,
cumulatively, the present studies indicate that the fish is a zooplankton feeder throughout all
# 2006 The Fisheries Society of the British Isles
its life stages.
Key words: Atherinopsidae; Chirostoma; cross-flow filtration; feeding; gill rakers; zooplanktivory.
INTRODUCTION
The Atherinopsidae are neotropical silversides which are principally marine
or estuarine, although some species occur in fresh water (Nelson, 1994; Dyer
& Chernoff, 1996). The genus Chirostoma is restricted to freshwater habitats
in altiplano lakes of central Mexico (Barbour, 1973), where it is geographically
†Author to whom correspondence should be addressed. Tel.: þ44(0) 1786 467882; fax: þ44(0) 1786
4712133; email: [email protected]
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isolated and hence unique. Chirostoma estor estor Jordan, known locally as
pez blanco, has for centuries been the basis of an artesanal fishery in Lake
Patzcuaro, Mexico. It is in great demand locally, has a high cash value and is
an important nutritional and financial resource for the fisher families of the
region. Yields have greatly decreased in recent years, due to overfishing, habitat deterioration and lack of fishery management. Because of its limited
range and declining numbers, it probably can be categorized as endangered
in terms of the IUCN classification, and this may also apply to some other
members of the genus, from which there have been extinctions in the last
few decades (Soto-Galera et al., 1998). Development of reliable culture technologies for this species would clearly be advantageous to enable its conservation through restocking as well as contributing to the livelihoods of
indigenous fishers.
Although the species has a great potential for aquaculture, the range of studies
of Chirostoma spp., has, to date, been limited and insufficient to establish
culture methods. One of the first accounts of culture of the genus was reported
by Rosas Moreno (1976), although the management and handling methods he
described gave limited success. Using basic aquaculture techniques, Armijo &
Sasso (1976) reported a 55% survival of larvae up to 12 days although subsequent feeding on Daphnia sp. gave only a 5% survival rate. Recently, significant progress in culturing C. e. estor has been made by Martı́nez-Palacios et al.
(2002a), who established appropriate handling techniques, evaluated optimum
temperature and devised a feeding sequence for the larval stages thus ensuring
high survival rates. Martı́nez-Palacios et al. (2004) noted the probable euryhaline ancestry of the group and designed a salinity regime for the hatchery
based on studies of salinity tolerances of the young stages, which substantially
improved survival, avoided fungal infestation and improved growth to the
juvenile stage. The current advances in biology and culture of the species were
summarized by Martı́nez-Palacios et al. (2006).
More research needs to be done, however, to understand feeding and nutrition of Chirostoma sp. and to optimize feeding strategies and diets for culture.
Studies of feeding structures, the alimentary tract and stomach contents have
frequently been used as a guide to feeding habits of a species (Lagler et al.,
1984). A prime example of such studies is that of Trewavas (1983) for the tilapia
genera Sarotherodon, Oreochromis and Danakilia. Sánchez & Rojas (1995) showed
that Chirostoma jordani Woolman was zooplanktivorous, feeding principally on
Bosminia sp., Daphnia sp. and Diaptomus sp. E. R. Moncayo & G. C. Escalera
(pers. comm.) showed that Chirostoma labarcae Meek also fed principally upon
the cladocerans Bosminia sp., Diaphanosoma sp. and Diaptomus sp. Solórzano
(1963) and Rosas Moreno (1976) determined the feeding habits of larvae of
C. e. estor based on gut contents and noted that they consumed ostracods, cladocerans and copepods. Stomach contents indicated that the adult stages of the
species may be piscivorous (Solórzano, 1963; Rosas Moreno, 1976).
There have been numerous studies of selective feeding in fishes although the
majority of such studies have been simply based on analysis of stomach contents. Few have related stomach contents to gill raker structure or gape size,
as in the case of Wankowski & Thorpe (1979), who showed that selective feeding
was size related in salmonids. Langeland & Nost (1995) studied a range of
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L. G. ROSS ET AL.
zooplankton-consuming fishes and found that the minimum and maximum size
of zooplankter ingested was independent of gill raker spacing. They concluded
that there was no clear relationship between the gill raker dimensions and prey
selectivity. More recently, Goodrich et al. (1999) and Sanderson et al. (2001)
proposed an alternative mechanism for zooplanktivory, cross-flow filtration,
which does not rely solely upon filter pore size and which may be more widely
applicable to fishes with a filter feeding strategy.
The present paper describes a series of experiments to identify the feeding
habits and strategy of C. e. estor at a range of ages and body sizes. The
basic feeding structures and body morphometry of the species are described
as well as the structure of the alimentary tract. The detailed morphological
arrangement, dimensions and development of the buccopharyngeal structures are described through optical and scanning electron microscope
(SEM) studies and these are correlated with feeding studies using natural
zooplankton.
MATERIALS AND METHODS
EXPERIMENTAL ANIMALS
Live adult C. e. estor were collected using a seine by commercial fishers in Tarério,
Ichúpio and San Jerónimo, Lake Patzcuaro, Michoacan, Mexico (19°370 N;
101°370 W), during June 2002. After transportation to the laboratory, eggs were fertilized and larvae were produced using the techniques described by Martı́nez-Palacios
et al. (2004).
The larvae were fed using the ‘Brachionis plicatilis–Artemia salina-balanced feed
sequence’ described by Martı́nez-Palacios et al. (2002a). Following weaning, stock
animals were grown on in the laboratory at 24° C using an artificial balanced diet to
provide a sequence of ages and sizes.
G E N E R A L M O R P H O M E T R Y O F C . E . E STO R
Two hundred and twenty seven individuals of C. e. estor from 3 to 270 mm standard
length (LS) were weighed following benzocaine anaesthesia (50 mg l1) and LS, head
height, ocular diameter, mouth gape (height), mandible length and length of intestine
were recorded to 05 mm using Vernier callipers (Pretul). The distance (mean of five
observations) between the base of the gill rakers was measured on the intact arch both
on gill arch 1 and on arches 2–4. Larvae and small individuals were examined using a
dissection microscope (WILD), fitted with an eyepiece graticule. Regression analysis
was carried out using MS Excel.
MORPHOLOGY AND HISTOLOGY OF THE ALIMENTARY
T R A C T O F C . E . E S TO R
Individuals of different sizes were dissected to confirm structure and probable functionality of different regions of the alimentary tract. Sections (5 mm) of alimentary tract
taken from a number of locations along its length were examined histologically following wax embedding and staining with haematoxylin and eosin, alcian blue, or periodic
acid-schiff (PAS) and Van Giesens.
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D E T A I L E D M O R P H O LO G Y O F T H E B U C C O P H A R Y N G E A L
A P P A R A T U S O F C . E . E S TO R
Dissection, washing and drying
The buccopharyngeal apparatus of 10, 20, 40, 80, 100, 360 and 720 day-old C. e. estor
was removed for examination. In adult specimens, this was achieved by cutting through
the mandibles in the mid-ventral aspect as far as the posterior limit of the opercula and
then dissecting forward from the junction of the pharyngeal teeth with the branchial
arches. For larvae and juvenile fish, a similar procedure was carried out with the aid
of iris scissors and a binocular microscope (Zeiss, Stemi DV4). Once extracted, the
structures were first cleaned in running water to remove excess blood and mucus. In
the case of larvae of 10, 20 and 40 days age, in which the buccopharyngeal structures
were too delicate to withstand more rigorous treatment, tissues were placed in a 10%
solution of sodium dodecyl sulphate for 3–4 h, following which they were washed to
remove loose tissue. Tissues from juveniles >40 days old were placed in a 10% solution
of sodium hydroxide for 1 h. The process was repeated up to three to four times depending upon size and was monitored using a Zeiss binocular microscope until the
overlying soft tissues were removed without destroying the buccopharyngeal apparatus.
Finally, all preparations were washed in distilled water and arranged in the required
position before oven-drying at 105° C for 24 h.
The cleaned and dried buccopharyngeal apparatus was examined using a dissection
microscope (WILD) and preliminary descriptions of the buccopharyngeal structures
were made.
Scanning electron microscopy
The prepared buccopharyngeal apparatus of 10, 20, 40, 80, 100, 360 and 720 dayold C. e. estor were mounted on an aluminium plate using double-sided adhesive tape.
The mounted samples were then coated in copper using a 20 min exposure in an
Edwards S150A sputter coater. Samples were examined using a JEOL JMS-6400 SEM.
For each age of fish examined, a collection of photographs was prepared, which included
the mandibular teeth, the branchial arches, the gill rakers and their ornamentation,
the pharyngeal pads and the pharyngeal teeth. Based on these sets of photographs,
descriptions and measurements (mean of five observations) were made of all of these
structures.
S E L E C T I V E Z O O P L A N K T I V O R Y O F C . E . E S TO R
To evaluate the ability of C. e. estor larvae to select prey, groups of 10 larvae aged
10, 20, 40 and 60 days were established, in triplicate, in 2 l plastic containers (38 14 13 cm). The containers were filled with previously aged water maintained at 25° C
range 1° C and a salinity of 5 (Martı́nez-Palacios et al., 2004).
A concentrated natural zooplankton mixture was obtained from earth ponds at the
Universidad Michoacana de San Nicolás de Hidalgo (UMSNH) by filtering 18 l of
pond water through a 50 mm mesh to produce a final volume of 650 cm3. A sample
(50 cm3) of concentrated zooplankton was fixed in formalin (40% formaldehyde solution) and retained for subsequent identification and quantification as far as order. The mixture comprised 275% ostracods (21 animals cm3), 541% cladocerans (41 animals cm3)
and 184% copepods (14 animals cm3).
The remaining 600 cm3 was then divided into 12 aliquots of 50 cm3. These were fed
to each replicate with thorough mixing in the container to ensure even distribution. The
fish were allowed to feed for 2 h, during which the feeding strategy was observed. The
fish were then killed in 50 mg l1 benzocaine, the LS, jaw gape and inter-raker distance
of all fish were recorded and they were then dissected under a binocular microscope
to extract the alimentary tract. The tract was then cut open and the contents were
identified and quantified to genus. The data were analysed in Excel using ANOVA
and Tukey’s test.
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L. G. ROSS ET AL.
RESULTS
G E N E R A L M O R P H O M E T R Y O F C . E . E STO R
Regression relationships for the principal body variables recorded are shown
in Table I. All regressions were highly significant (P < 005). In terms of feeding structures, the relationship between LS and mouth gape and size of mandibles remains linear up to the maximum size and age examined (Table I). The
length of the alimentary tract relative to LS also remains constant up to the
maximum size and age examined. The ratio of alimentary tract length to LS
is relatively small at 029:1.
MORPHOLOGY AND HISTOLOGY OF THE ALIMENTARY
T R A C T O F C . E . E S TO R
Chirostoma estor estor has a relatively small, superior, protractile mouth with
a maximum gape of 21 mm in 22 cm LS adults. Unicuspid teeth occur on the
upper premaxilla and are arranged in three rows. The lower mandible has four
rows of simple, conical, unicuspid teeth which are small and fragile. These observations are indicative of a pelagic predator feeding on small prey.
The alimentary tract in C. e. estor is a simple relatively undifferentiated
looped structure. The oesophagus is a short muscular tube, which has a gently
folded mucosal epithelium, stratified in the anterior portion but stratified and
simple in the posterior portion. The epithelial cells contain mucus-like substances in the cytoplasm and the submucosa is composed of connective tissue
somewhat denser than that of the lamina propia.
The intestine consists of three sections: anterior, posterior and the rectum.
There is no evidence of a stomach, localized thickening, augmentation of
musculature or presence of pyloric caecae at any of the ages examined. The
anterior section, to which the bile ducts are connected, occurs before the loop
of the tract and is analogous to the duodenum. The posterior part of the intestine is more muscular after the loop. The intestinal mucosa is composed of
TABLE I. Relationships between morphometric variables and standard length (LS) of
Chirostoma estor estor
Relationship
Log10 ocular diameter and log10 LS
Log10 vertical jaw gape and log10 LS
Log10 upper mandible length and
log10 LS
Log10 lower mandible length and
log10 LS
Log10 anterior gill raker spacing and
log10 LS
Log10 head height and log10 LS
Log10 length of alimentary tract and
log10 LS
#
Equation
n
P
r2
y ¼ 111 þ 0945x
y ¼ 105 þ 112x
y ¼ 116 þ 116x
268
222
217
<0001
<0001
<0001
0986
0994
0993
y ¼ 117 þ 115x
217
<0001
0981
y ¼ 168 þ 0814x
72
<0001
0936
132
213
<0001
<0001
0956
0983
y ¼ 0842 þ 098x
y ¼ 0568 þ 114x
2006 The Fisheries Society of the British Isles, Journal of Fish Biology 2006, 68, 1782–1794
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1787
a single layer of high columnar epithelial cells which contains scattered goblet
cells. The mucosal folds are deep along the length of the intestine to the rectum
where the folds become shallow. The rectum also has thickened muscle layers.
MORPHOLOGY OF THE BUCCOPHARYNGEAL APPARATUS
O F C . E . E S TO R
The structure and conformation of the branchial basket is a conspicuous
feature of the ventral buccal cavity of C. e. estor [Fig. 1(a)]. The first gill arch
has two types of gill raker. The anterior side of the arch has long rakers which
are anteriorly directed [Fig. 1(b)]. These develop in length with age and start to
produce a row of spine-like lateral processes as the fish approach 100 days old
[Fig. 1(d)]. The rakers become more numerous as the animal continues to grow
and the spines also increase and become a double row in older specimens
[Fig. 1(b), (c)]. Gill arch 1 also has a row of smaller rakers, which are identical
to the two rows of smaller rakers that occur on gill arches 2–4 [Fig. 1(b)]. These
structures appear initially as simple, low profile pads, which develop spines and
become progressively more elaborate as the animal grows. The adult form of
these pad-like rakers spans the entire interior surface of the gill arch (Fig. 2).
The spacing of the long rakers on gill arch 1 is greater than those on the
other arches and both spacings increase with age (Table II and Fig. 2). The
number and length of the rakers of both types also increase with age (Table II),
although rakers on arch 1 are up to five times longer than those on arches
2–4. The number of spines on the rakers also increases with age. Careful
manipulation of the isolated branchial basket revealed that the pads on arches
2–4 interdigitate accurately, forming a filter constructed of a continuous mat of
spiny pads (Fig. 2). The simultaneous growth and development of the spiny
FIG. 1. Scanning electron micrographs showing development of gill rakers in Chirostoma estor estor. (a)
The branchial sieve, (b) short rakers on gill arches, showing development of spines with age, (c) long
rakers on first gill arch and (d) processes on long rakers.
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FIG. 2. The gill rakers on Chirostoma estor estor, showing the long rakers on arch 1 (left), the close
interdigitation of the pad-like rakers on arches 1–4 forming a spiny filter mat (centre) and the
pharyngeal teeth (right).
pads on gill arches 2–4 ensures that a continuous filter of spines is maintained
throughout development. This flexible mat of spines appears to constitute the
principal filtration apparatus of the species.
The species possesses notable dorsal and ventral pharyngeal teeth (Fig. 3),
although these are rudimentary in the early stages. The pharyngeal pads
TABLE II. Characteristics of the gill rakers with age in Chirostoma estor estor. Measurements are the mean of five observations from individual specimens
Number
of rakers
per arch
Length
of rakers
(mm)
Inter-raker
distance
(mm)
Number
of spines
per raker
Length of
spines
(mm)
Interspine
distance
(mm)
Gill arch 1
10
62
20
81
40
115
80
20
100
29
360
78
720
164
0
13
13
15
15
23
26
—
93
135
374
630
1536
2159
—
37
50
65
93
266
581
—
0
0
0
3
40
40
—
—
—
—
36
71
173
—
—
—
—
73
70
78
Gill arches 2–4
10
62
20
81
40
115
80
20
100
29
360
78
720
164
0
0
0
18
23
27
36
—
—
—
65
93
286
755
—
—
—
70
102
207
397
0
0
0
2
3
11
20
—
—
—
27
32
71
160
—
—
—
11
15
30
54
Fish age
(days)
#
LS
(mm)
2006 The Fisheries Society of the British Isles, Journal of Fish Biology 2006, 68, 1782–1794
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FIG. 3. Scanning electron micrographs showing the development of the pharyngeal teeth with age in
Chirostoma estor estor. D, dorsal pharyngeal teeth; V, ventral pharyngeal teeth.
develop conspicuously as the fish grow and adults have large numbers of sharp
unicuspid teeth with rows of larger molariform teeth on the posterior edge of
the ventral pad (Fig. 3).
S E L E C T I V E Z O O P L A N K T I V O R Y I N C. E. ESTO R
Chirostoma estor estor of all sizes were observed to capture prey items by a process of selective biting. The jaw teeth are not involved in seizing prey items and
it is probable that multiple items are seized on each bite. In general, juvenile
C. e. estor of different ages consumed mixtures of ostracods, cladocerans and copepods from the zooplankton mixture, regardless of fish age (Fig. 4). There was
a difference in the size range of prey items with age. Ten day-old larvae consumed principally ostracods up to 280 mm diameter, few cladocerans and no copepods. Twenty and 40 day-old larvae consumed all three groups of zooplankton
up to 500 mm or more. Sixty day-old juveniles also consumed all three groups
but with an emphasis on copepods and up to 700 mm in length (Fig. 4).
The increase in mean size of prey items is summarized in Table III. The
trend is generally significant in the case of ostracods and copepods, but is less
clear in the case of cladocera. The increase in prey size with age is paralleled by
an increase in jaw gape and gill raker spacing (Table III).
TABLE III. Mean maximum length of zooplankters in the alimentary tract of Chirostoma
estor estor
Fish age
(days)
LS
(mm)
Ostracoda
maximum
length
(mm)
10
20
40
60
59
112
156
214
1263a
1366a
1150a
1796b
Cladocera
maximum
length
(mm)
Copepoda
maximum
length
(mm)
Vertical
jaw gape
(mm)
Inter-raker
distance
(mm)
1970a
2962b
1963a
2564ab
n.d.
3016a
2740a
3719b
048
098
157
216
n.d.
40
50
68
Number of observations at each age ¼ 30. Values with the same superscript lowercase letters are not
significantly different (P 005). n.d., not determined.
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200
(a)
150
100
50
60 Days
40 Days
20 Days
10 Days
0
0
200
100
200
300
400
500
600
700
800
(b)
100
50
60 Days
40 Days
20 Days
10 Days
0
0
100
200
300
400
500
600
700
Age
Number of organisms
150
800
(c)
200
150
100
50
60 Days
40 Days
20 Days
10 Days
0
0
100
200
300
400
500
600
700
800
Diameter (µm)
FIG. 4. The relationship between the number and size of zooplankters (a) ostracods, (b) cladocerans and
(c) copepods consumed by Chirostoma estor estor of different ages.
DISCUSSION
Filter feeding is a broad term which describes a wide range of strategies for
capture and retention of small prey items, and for which a wide range of structural and tactical arrangements have evolved (Hoogenboezem et al., 1991;
Hart, 1997). In the present trials, the prey items appeared to be identified visually and were captured by a biting action. It is not clear, however, whether this
is a true biting action, in which the teeth of the upper and lower jaws are used
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to capture food, or whether prey is simply being ‘sucked’ into the buccopharyngeal cavity (Liem, 1991). Individual or multiple items may be captured in each
biting action. Chirostoma estor estor has a relatively small head with a limited
vertical jaw gape (Table I) and the fine unicuspid jaw teeth, pharyngeal teeth
(Fig. 3), simple relatively short alimentary tract and lack of stomach or pyloric
caecae are all indicative of a continuous feeder accessing abundant and highly
digestible prey.
In the early stages of development the filter structures are extremely simple,
but the branchial basket, gill rakers and their spines continue to develop in
complexity with age (Fig. 1). The gill raker spacing and interspine distances
also increase with age. The fact that younger animals ingest smaller prey
while older animals consume larger prey (Fig. 4) may be related to these
changes in feeding structures. Differences in prey ingestion with age, however,
may also reflect changes in fish swimming abilities. Overall, these structural
arrangements are similar to those of other plankton feeders, such as the
clupeoids, although targeted on larger prey items. Although phytoplankton
feeders appear to be obligate, it is probable that all zooplankton feeders are
in fact facultative, with the ability to modify capture strategy depending upon
prey density, prey size and light intensity (Bone et al., 1995) and to switch to
feeding on single prey items when necessary or advantageous. Various authors
have described the feeding habits of C. e. estor based solely upon examination
of stomach contents. There is a differential rate of digestion of the prey organisms in zooplanktivores and extreme care needs to be taken to ensure that samples are not biased because of this factor. When very young, up to 20 days old,
C. e. estor are probably general particulate feeders as gill raker development is
extremely simple. Above this size, the rakers and spines develop markedly,
eventually with considerable complexity, and the fish retain prey by filtration,
a feeding mode which does not preclude opportunistic ingestion of other prey
items (Solórzano, 1963; Rosas Moreno, 1976).
Chirostoma estor estor consume small fishes as part of the process of capturing
zooplankton and small fishes have previously been recorded occasionally in the
gut contents (Solórzano, 1963; Rosas Moreno, 1976). Although they are principally zooplanktivorous, adult C. e. estor are also capable of switching to an
opportunistic feeding strategy as the mouth gape is large enough to take small
fishes and crustaceans. It is possible that this switch in feeding mode from zooplankton selection to opportunistic piscivory may be triggered during seasons in
which plankton biomass is relatively low. Fishes are digested less easily than
most zooplankters and so can consequently assume a level of importance in
gut examinations which is greater than their real status. Sutela & Huusko
(1999) proposed that bias can be avoided by examining only foregut contents.
Based on detailed anatomical studies using SEM and experimental studies in
which fish were fed on zooplankton mixtures, the mechanism of prey retention
of the species can now be proposed. The gill arches, especially arches 2–4,
posses a series of interlocking spiny pads, which form a flexible, spiny filter
mat in the buccal cavity (Fig. 2). While analysis of the size of prey items trapped
and comparison with the spacing of the pads and their adorning spines and interspine distances suggest that this could be a simple dead-end filter in small
fish (Tables II and III), this is not the case for older animals. In a dead-end
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filter, smaller particles pass through and are lost in the filtrate, which has the
disadvantage that it becomes blocked by the ‘retentate’ with time (Hessen et al.,
1988; Sanderson et al., 1998; Goodrich et al., 1999).
The buccal structures of C. e. estor have many of the characteristics of a
cross-flow filter, a mechanism that is widely used in numerous industrial processes for recovery of particles ranging from sewage sludge to yeast cells to fine
colloids. Working with non-biological cross-flow systems, Sibanda et al. (2002)
showed that some of the flow passes directly through the filter, depositing particles on the surface as in a normal dead-end filter. The major flow, however, is
parallel to the filter surface and particles aggregate together on the surface of
the filter forming aggregates, which are much larger than the apparent pore
size. In addition to delivering particles to the filter bed, this transverse flow also
sweeps over the filter surface shearing the aggregated particles clear of the bed.
This results in accumulation of aggregated particles downstream of the filter,
which can then be removed from the flow and collected.
In fishes, the initial deposition of zooplankton on the filter bed and their subsequent aggregation into larger particles is probably assisted by mucus (Sanderson et al., 1991, 1996). The aggregated particles are then cleared from the filter
surface by the cross-flow pattern of currents. Cheer et al. (2001) derived flow
models based on endoscopic observations to demonstrate that such a flow pattern existed in Nile tilapia Oreochromis niloticus L., a particulate feeder which
possesses pharyngeal teeth and employs hydrosol filtration. In fishes, clearing
of the filter bed may further be assisted by the fact that, unlike industrial filter
beds, the filter surface flexes during normal ventilatory movements. There
could also be a strong contribution from periodic flow reversals in fishes, such
as coughing, which in many species occurs once or twice per minute (Ross
et al., 1985). Cumulatively, these processes could keep the filter permanently
clear and unblocked. The aggregated feed particles are swept towards the back
of the buccal cavity by the flow pattern in the cavity, becoming progressively
more concentrated as the material moves over the filter bed and as excess water
passes out through it. In this way, the food aggregates are presented in a concentrated form to the pharyngeal teeth at the back of the buccal cavity, where
they are pre-ground before passing into the stomachless alimentary tract to be
broken up by powerful enzymes. Recent studies have shown that C. e. estor has
high levels of trypsin-like enzymes, operating at high pH and these are well
suited to digestion of triturated zooplankton in a stomachless fish (Martı́nezPalacios et al., 2002b).
The present study illustrates that reliance on analysis of gut contents to
determine feeding abilities or feeding niche is unreliable. Although the feeding
structures, gut anatomy and digestive enzymes of C. e. estor are all indicative of
a zooplankton feeding strategy throughout the life cycle, the species also has
the ability to consume larger organisms opportunistically (Solórzano, 1963;
Rosas Moreno, 1976). Care must be taken in determining feeding niche from
gut contents alone as some material, such as zooplankton, are much more
readily digested than fishes or plant material potentially leading to erroneous
attribution. This work provides valuable data on which to base design of feeds,
feed delivery systems and feeding strategies for development of successful aquaculture of the species.
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2006 The Fisheries Society of the British Isles, Journal of Fish Biology 2006, 68, 1782–1794
F I L T R A T I O N A N D Z O O P L A N K T I V O R Y I N C H I RO S T O M A
1793
Thanks are due to CONACyT for financial support for this research and to the Darwin
Initiative (DEFRA, U.K. Government) for link support. We extend our thanks to the
Instituto de Metalurgia (UMSNH) for access to their SEM facilities and to S. Abad
Rosales for histological support.
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