-
Environmental Biology of Fishes 26: 177-199. 1989.
@ 1989 Klu~'er Academic Publishers. Printl'd in thl'
Netherlands
Ontogenetic diet shifts and resource partitioning among
piscivorous fishes inthe Venezuelan llanos
Kirk O. WinemillerDepartment of Zoology, The University of
Texas, Austin, TX 78712, U.S.A
Accepted 12.12.1988Received 18.8.1988
Key words: Caquetia, Charax. Diet breadth, Diffuse competition,
Gymnotus, Hoplias. Resource overlap,Piranha, Pygocentrus, Rhamdia.
Seasonality, Se"asalmus
Synopsis
Resource utilization by nine abundant piscivores from a diverse
tropical fish assemblage was examined overthe course of a year. All
nine species exhibited peak reproduction during the early wet
season and a similarsequence of size-dependent shifts from a diet
composed primarily of microcrustacea, to aquatic insects,
andfinally fishes. Three piranha species specialized on fish firis,
particularly at subadult size classes (SL30-80mm). Gradual
dessication of the floodplain during the transition season was
associated with fishgrowth, increased fish density, and decreased
aquatic primary productivity and availability of invertebrateprey.
Based on 118 resource categories, average pairwise diet overlap was
low during all three seasons: wet,transition, and dry. Of 72
species pairings, only one pair of fin-nipping piranhas exhibited
high overlapsimultaneously on three niche dimensions: food type,
food size, and habitat. Adults of two species, agymnotid knifefish
and pimelodid catfish, were largely nocturnal. Patterns of habitat
utilization indicate thatpiranhas may restrict diurnal use of the
open-water region by other piscivores. Collective diet overlap
ofindividual piscivore species with the other eight feeding guild
members and collective overlaps with the entirefish community each
revealed two basic seasonal trends. Four species that showed an
early switch topiscivory also showed a high degree of diet
separation with both the guild and community at large on
ayear-round basis. The five remaining species showed lowest
collective diet overlaps during the transitionseason when
availability of invertebrates was reduced and fish densities were
maximal. Whereas predationmay playa role in habitat separation,
diffuse competition for food resources during the
approximatelyfour-month transition season probably is the principal
factor yielding patterns of diet specialization.
bers provides the most straightforward means ofattaining a
preliminary assessment of the relativeimportance of interactive
processes within naturalcommunities. Whereas descriptive studies
that re-veal patterns of resource subdivision are limited intheir
abilities to demonstrate the mechanisms cre-ating observed
relationships (Toft 1985), thought-ful comparisons and the weight
of evidence derivedfrom numerous studies already have yielded
muchinsight (Schoener 1974, Helfman 1978, Sale 1979,
Introduction
Most diverse taxonomic groups of organisms ex-hibit divergence
in trophic biology (e .g., cichlidfishes, Greenwood 1981;
ostariophysan fishes,Fink & Fink 1981). Whether or not
ecomorpholog-ical divergence is random or adaptive in the contextof
community interactions can be debated (Stronget al. 1979, Grant
1981). The study of resourceexploitation among syntopic feeding
guild mem-
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178
focuses on the piscivore guild as a potential unit
forcompetitive biological interactions. Given the cli-mate and
natural history of the Cano Maraca eco-system, several basic
questions can be asked: (1)Do piscivorous fishes partition food and
habitat,and if so, what is the influence of seasonal changesin
their environment? (2) What are the relation-ships between
ontogeny, resource partitioning,and seasonal changes in resource
availability? (3)Given seasonal patterns of resource
availabilityand exploitation by consumers, is there evidence
ofinteractive effects on piscivore feeding behavior?(4) Do seasonal
trends of pairwise species dietoverlaps follow patterns from
collective diet over-laps within the piscivore guild or total fish
commu-nity, and if not, which index offers a better assess-ment of
the likelihood of interactive effects?
Methods
Study site
During every month of 1984, fishes were collectedfrom Calio
Maraca, a swamp-creek of the RioApure-Orinoco drainage in the
western llanos ofVenezuela (8° 52' 30" Lat. N; 69°27' 40" Long.
W).The region studied (termed an 'estero') lies withinlow, flat
terrain that experiences extensive sheetflooding during the wettest
months (late May-Au-gust). During this time, a large region
borderingthe creek channel is converted from exposed, sun-baked
soil and thorn-scrub habitat into a produc-tive marsh with diverse
aquatic vegetation dom-inated by Cyperus sp., Eichhornia
diversifolia, andHeteranthera reniformis. During the driest
months(Dec.-May), the aquatic habitat is reduced to anetwork of
mud-bottom pools blanketed by Pistiastratiotes, Salvinia spp., and
Lemna spp.. Dis-solved oxygen concentrations are reduced at
thistime and many fishes rely on special respiratoryadaptations for
survival. Annual rainfall in the re-gion was 1300 mm during 1984,
with 860 mm fallingbetween June and September (Fig. 1). Based
onchanges exhibited by stream physico-chemicalparameters associated
with rainfall and their ef-fects on aquatic organisms (Winemiller
1987a,
Werner 1979. Toft 1985). In a recent review of theliterature on
fishes. Ross (1986) observed greatestpartitioning on food
dimensions. followed by hab-itat and time. Many studies treating
two or moreniche dimensions have shown complementarity. in-dicating
a potential effect of interspecific competi-tion. An interactive
effect between competition.predation, and temporal shifts in
abiotic environ-mental parameters has been suggested for
somesystems (Werner & Hall 1977, Werner et al. 1983,Mittlebach
1984. and see Schoener 1974. Toft1985). Ross (1986) observed a
general pattern ofstudies revealing less evidence of interactive
effectson community structure in harsher environments.
Seasonal changes in resource availability and on-togenetic diet
shifts can affect both predator-preyand competitive interactions
among size-structur-ed fish populations. The present study
exploresseasonal and size-related patterns of resource
ex-ploitation within the piscivore guild of a diverseneotropical
fish community. Although varyinggreatly in both duration and
breadth of taxonomiccomparison, several recent studies have
shownmarked resource partitioning among tropical fishes(Angermeier
& Karr 1983, Power 1983, Moyle &Senanayake 1984, Schut et
al. 1984, Watson &Balon 1984, Araujo-Lima et al. 1986, Hyslop
1986,Prejs & Prejs 1987, Nico & Taphorn 1988).
Fishpopulations frequently are size structured due tosmall hatching
or neonate size and continuousgrowth. Body size significantly
affects the sizerange of food particles potentially available to
con-sumers (Brooks & Dodson 1965. Werner 1974,Magnan &
Fitzgerald 1984). Furthermore, size dis-tributions of fish
populations directly influencepredation rates on different age
classes and oftenthe spatial distribution of fishes (Fraser &
Cern1982, Mittlebach 1984, Power 1984, Werner & Gil-liam
1984).
The study site, Calio Maraca, experiences highlyseasonal
rainfall that is characteristic of many partsof central and
southern Venezuela. Most fishesreproduce during the early and peak
wet season, asituation that leads to temporal changes in
averagebody size for most species (Winemiller, unpublish-ed).
Although similar data were collected for allfishes that occurred at
the site, this investigation
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179
. . .. ....10. ,.. -0' A~, _0' .lu. .lul ... 00' Mo. 0..
Fig. 1. Average monthly rainfall (closed symbols) and
maximum
midpool depth measured each month (open symbols) during thestudy
period at Cano Maraca.
1987b), the annual cycle was divided into threeterms of equal
duration: dry season (Jan.-Apr.),wet season (May-Aug.), and
transition season(Sept.-Dec.). Dry season conditions gave way tothe
wet season very abruptly with the commence-ment of heavy rains,
whereas the wet season slowlygraded into the next dry season over a
prolongedperiod (i.e., transition season). During the transi-tion
season, fish densities increased and biotic in-teractions
intensified within gradually diminishingaquatic habitats in the
floodplain. Estimates of fishbiomass at Cano Maraca at the end of
the transitionseason are among the highest densities recordedfor
natural freshwater ecosystems (141-165g m-2,Winemiller 1987a). All
available climatic and ec-ological information indicate that 1984
was not un-usual in the sequence or magnitude of events.
Forexample, the rainy season sometimes begins earlieror later than
the last week of May, yet the first rainsare typically heavy,
persist for several months,slowly subside, and nearly cease all
together forseveral months during the peak dry season.
three wet months, collecting effort expended wasapproximately
equal during each sampling period.More total time was spent
collecting during the firstthree months of the wet season due to
the compara-tive inefficiency of adult fish captures in the
newly-expanded aquatic environment. All aquatic hab-itats in the
estero region were sampled for a mini-mum of six hours (habitats
combined), and a col-lecting outing was terminated when two hours
ofsampling yielded no additional species. Collectionsused for
comparisons of relative densities weremade during either one or two
days between the11th and 28th of each month. Additional
collec-tions were made on other dates to supplement stan-dard
samples of uncommon species. A completelisting of collecting dates
and sample sizes for pre-served specimens appears in Winemiller
(1987a).Collecting activities should not have affected nat-ural
fish densities between sampling periods, be-cause (1) only a
fraction of the total aquatic habitatwas sampled on a given date
and (2) fishes couldmove freely between the estero region and
thepennanent channel downstream (except duringMarch and April). All
collected individuals werepreserved in 15% formalin rather than the
usual10% to safeguard against decomposition of stom-ach contents.
The largest fishes were cut on thelateral wall of the visceral
cavity to hasten pene-tration of formalin. Following examination, a
por-tion of the fishes collected was deposited with theMuseo de
Ciencias Naturales de UNELLEZ, Gua-nare, Portuguesa, Venezuela. The
remainder wasdeposited in the Natural History Collection of
theTexas Memorial Museum, University of Texas,Austin, Texas.
Separate samples were taken on 27 and 28 Sep-tember, 25 and 26
October, 22 November, and IIDecember from three habitats: open
water mid-pool (day and night), shallow pool edge, and
densevegetation. The open water habitat was sampled ina large pool
at the lower end of the estero with the20m, 12.7mm mesh seine.
These large seine sam-ples were preserved in 15% formalin and kept
sep-arate from small seine (2.5 m, 3.17mm mesh) sam-ples taken from
the same pool. Because the largemesh seine allowed small fishes to
pass through,and large fishes easily avoided the small seine,
Collections
Fishes were collected by seine (3.17mm un-stretched mesh. 2.5m
length; 12.7mm mesh. 20mlength). experimental gillnet. and dipnet.
On eachouting. an attempt was made to sample the entirefish
community such that the sample for each spe-cies reflected its
relative abundance and size struc-ture during each month. With the
exception of
!~i..0
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180
values obtained for the number of individuals ofeach species in
the two open water samples werelater combined as one sample. Night
samples weretaken from the same open water location with bothseines
on 27 September and 25 October (1800-2400 h). The 2.5 m seine was
used to sample openand sparsely vegetated, shallow shoreline
habitatduring the morning of each outing. For the vegeta-tion
habitat samples, the 2.5 m seine was rolled onpoles attached to
each end until the total area ofexposed net was 4.2 m2. The
weighted end of theseine was passed below dense masses of
floatingvegetation and quickly brought to the surface onthe other
side, enveloping a quantity of aquaticvegetation approximately
equal to the area of theseine and entrapping all fishes contained
therein.The vegetation was then hauled to the adjacentshoreline
where fIShes were extracted and pre-served.
Diet analysis
for stomach content analysis. For certain piscivo-rous species,
such as Hop/ias ma/abaricus and Py-gocenlrus nolalus, all available
specimens were dis-sected. When more than 30 specimens were
avail-able, a subsample was chosen for dissections thatincluded
representatives spanning the total spec-trum of size classes in the
collection. During thecourse of one year, 83 fish species were
collectedfrom the estero. Each monthly sample producedbetween 40
and 60 species (Winemiller 1987a).This paper reports findings for
the nine most abun-dant piscivorous species only: Hop/ias
malabaricus(Erythrinidae), Charax gibbosus (Characidae),Pygocenlrus
nolalus (Characidae), Serrasa/mus cf.irritans (Characidae),
Se"asalmus cf. medini, Ser-rasalmus rhombeus, Gymnolus carapo
(Gymnoti-dae), Rhamdia sp. (Pimelodidae), and Caqueliakraussii
(Cichlidae). For the purposes of this study,piscivores were defined
as fishes averaging at least50% fish prey in the diet of the
largest adult sizeclass. Six piscivorous species were rare in the
localecosystem and omitted from the analysis [i.e.,
Ac-eslrorhynchus microlepis (Characidae), Ageneio-sus brevifilis
(Ageneiosidae), Crenicich/a saxalilis(Cichlidae), Hoplerylhrinus
unilaeniaIUS (Erythri-
nidae), Pseudoplalysloma fascialum (Pimelodi-dae), and
Slernopygus macrurus (Sternopygidae»).Additionally, four common
species that consumedfishes in minor proportions were excluded from
thecomparisons [Aequidens pulcher (Cichlidae), As-lronOIUS
ocellalus (Cichlidae). Parauchenip'erusgalealus (Auchenipteridae),
and Synbranchus mar-moralus (Synbranchidae) J.
Food items in the anterior half of the gut wereremoved, examined
under a dissecting microscope,and identified at the species
(fishes) or ordinal level(invertebrates). Broader food categories
were notused for numerical analyses, because (I) lower tax-onomic
categories generally represented one ormore renewable resources,
and (2) lumping re-source states often inflates niche overlap
values(Greene & Jaksic 1983). Prey items then were sort-ed,
carefully blotted with a dry paper towel, andwhile still moist,
measured in an appropriatelysized graduated cylinder by water
displacement.The degree of resolution for very small items was0.005
mi. For volumes less than 0.005 ml, a value
All preserved specimens were identified, counted,and measured
for standard length to the nearest0.1 mm (alliengtbs are reported
hereafter as SL).Fisb species names were provided by Donald
Ta-phorn of UNELLEZ and Francisco Mago-Lecciaof UCV (Caracas). and
voucher specimens areavailable in the Museo de Historia Natural
(UN-ELLEZ) and The Texas Natural History Collec-tion (TMM. UT,
Austin). Many Venezuelan spe-cies could not be given tentative
species names dueto the current state of taxonomic confusion.
Conse-quently, a few species were designated as distinctforms by
'sp.'. Two piranhas were initially identi-fied as Se"asalmus
eigenmanni and Serrasalmussp. (Taphorn & Lilyestrom 1985). The
piranha sub-family (Serrasalminae) is currently under
revision.According to William L. Fink (personal communi-cation).
these species correspond to Se"asalmuscf. irritans and Se"asalmus
d. medini, respective-Iy. Caquetia kraussii was formerly listed as
Peteniakraussii (Mago-Leccia 1970. and see Kullander
1983).Whenever available, 30 specimens of each spe-
cies from each monthly collection were dissected
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181
was estimated by spreading the item on a glass slideand
comparing it to a similarly spread substanceknown to equal 0.005
mi. Except for highly frag-mented material. the size interval
associated witheach identified prey item was recorded (10mm
in-tervals measured along the longest particle axis).An ocular
micrometer aided linear measurementsof small prey items. Diet
breadths were calculatedby Simpson's measure (Simpson 1949).
Asymmet-rical diet overlaps were calculated by MacArthur
&Levins' (1967) formulas:
mirrors the feeding habits of the population atlarge. This study
employed niche overlap (fp) as ameasure of similarity only, and not
as a direct esti-mate of interspecific competition (a) in the
mannerpreviously used by some investigators.
Following the method of Lawlor (1980), electiv-ities were used
in place of Pi~ for an additional setof diet overlap measures
adjusted for prey relativeabundances (hereafter referred to as diet
similar.ities). Consumer electivities (ei,) were calculated as
Pi/e= Rb' '/I
(fJik = --'-
.L P;/'IAI~I -.
L plj2i-I
and
fit! a
.I: PtIJ~I-I
.r P1.2I-I
where Pij is the proportion of prey item i consumedbyspeciesj.
andpik is the proportion of the ith preyitem consumed by species k.
These measures re-flect differences in the magnitude of overlap
be-tween two populations due to unequal nichebreadths. For example,
one would expect dietoverlap of the more specialized bluegill
sunfish.Lepomis macrochirus. on the green sunfish. L.cyanellus. to
be less than that of the latter on theformer (Werner & Hall
1977). The asymmetricalmeasure has been viewed as desirable in the
sensethat potential for exploitation competition for re-sources is
more realistically portrayed as unequalfor species having different
diet breadths (Slobod-chikoff & Schulz 1980). Whereas this and
othermeasures of niche overlap present difficulties forstatistical
inference when three or more species arecompared. they at least
provide a simple. reliableindex of diet similarity. All PijS were
based on thetotal volumes of the food items consumed during
aspecified period. This method assumes that stom-ach contents from
a large sample of individuals
where Rj is the relative proportion of food item i inthe
environment, and pjj is the proportion of item;in the diet of
consumer species j. The relative abun-dance of each prey item in
the environment wasestimated from the column sums in the
communityresource matrix (items summed across all fish spe-cies
examined, both piscivorous and nonpiscivo-rous). Although it is
labor intensive, this method ofcalculating Rj has the advantage of
basing total preyavailability on the overall performance of the
en-tire fish community. Assessment of prey R;s basedon independent
sampling efforts risk (1) under-estimating availability when
microhabitats avail-able to fish are undersampled, and (2)
overestimat-ing availability when large numbers of prey that
areactually invulnerable to predation are sampled(Wallace 1981). In
effect, the method estimatesfood availability using fishes rather
than humans assamplers of their environment. The method ismore
reliable when based on diverse assemblagescontaining many
ecomorphotypes, because anysingle species would have a relatively
small influen-ce on estimates of availability.
Ecological measures and statistics were comput-ed from the three
seasonal resource matrices (9predators x 118 potential prey
categories). Foranalysis of ontogenetic diet shifts, dissected
speci-mens were grouped into either 10 or 20 mm in-tervals,
depending on the total range of SLs record-ed for each species. The
average proportion ofmicrocrustacea, aquatic insects, and fish prey
itemswas determined for each fish size interval. Fishscales were
omitted from this analysis, because
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182
scales comprised a minor portion of diets and noneof the nine
species are believed to rely on scales as asignificant food
resource (sensu Roberts 1970, Sa-rima 1983). Most scales not
associated with fleshwere probably taken during aggressive
interactionsby these species. All statistical tests were computedby
SAS (SAS Inst. 1985). A generalized linearmodel (GLM) procedure was
used for calculationof ANOVA statistics for comparisons of data
setswith large unequal sample sizes.
ta argentea. numerically dominated the estero
(Winemiller 1987a).Average size of all nine piscivores was
greater
during the transition season than the wet seasondue primarily to
growth of juveniles produced dur-ing June and July (Fig. 2).
Hoplias. Charax, Pygo-centrus, Gymnotus, and Caquetia were
extremelyabundant within shrinking aquatic habitats duringthe
transition season. Populations of Hoplias,Charax, and Caquetia
consisted of a mixture ofadults, subadults, and juvenile size
classes duringthe transition season. Both adult and subadult
sizeclasses of Rhamdia and Gymnotus were taken dur-ing the
transition season, whereas the four piranhaspecies primarily
consisted of subadults. Duringlate October, dissolved oxygen
concentration ex-hibited a temporary reduction (mean dissolved0] =
0.73 ppm), which probably resulted from apulsed increase in total
microbial metabolism asso-ciated with the death of aquatic
macrophytes inshallow standing waters of the drying
floodplain(Winemiller 1989). At this time, all four piranhaspecies
were rare or absent from the estero regionof Cano Maraca. The four
species reappeared onthe site after dissolved oxygen had increased
withinthe stream channel (0] = 2.s-6.0ppm) within sixweeks.
Young-of-the-year Pygocentrus (76-127 mm) were taken in large
numbers during No-vember and December (Fig. 2).
Results
The piscivore guild of the dry season was dom-inated by adult
Hop/ias ma/abaricus, followed byCaquetia kraussii (17-185 mm),
adult Gymnotuscarapo. and adult Rhamdia sp. (Fig. 2). During
theharshest months of the dry period (Feb.-earlyMay), Charax
gibbosus and the four piranha spe-cies (Pygocentrus and Se"asalmus
spp.) emigratedfrom the estero region to deeper aquatic
habitatsdownstream. Collections made on Caito Maraca ata location
14km east (downstream) of the esteroduring the height of the dry
season yielded severalindividuals of Charax. Se"asa/mus irritans,
and S.medini. Small juveniles of Hop/ias and especiallyCaquetia
were taken at various intervals during thefour month dry season,
indicating that at least por-tions of the local populations were
reproductivelyactive.
Charax, Pygocentrus, and S. irritans returned tothe estero
within one week of the abrupt onset ofthe rainy season. All
individuals of these speciestaken during June were adults with
gonads in ad-vanced states of maturation. Eleven large
malePygocentrus in black nuptial coloration were takenin shallow
water among emergent stands of aquaticmacrophytes with one haul of
the 2.5 m seine onJune 6. Each male had milt-laden testes, and
theirstomachs contained either large cycloid scales orplant debris.
Juveniles of all nine species were col-lected during July and
August. During the wetseason, small omnivorous and herbivorous
char-acids (especially Astyanax bimacuJarus. Markianageayi.
Ctenobrycon spi/urus, and Odontosti/beDu/cher), and the
detritivorous curimatid, Curima-
Ontogenetic diet shifts
Of m9 specimens from Cafio Maraca that weredissected for diet
analysis, the nine major pisci-vores comprised 1980 (20%). Small
juveniles of allnine species exploited aquatic microcrustacea
andaquatic insects (Table 1, Fig. 3). Pygocentrusshowed two
distinct ontogenetic shifts in basic dietcomponents: from primarily
microcrustacea to aq-uatic insects (20-40 mm), and from aquatic
insectsto fishes (4()...()() mm). Rhamdia experienced similardiet
shifts between 2a-40 mm and ro-so mID re-spectively. A mixture of
microcrustacea and aquat-ic insects dominated the diets of juvenile
Hoplias«50mm), S. irritans «30mm), S. medini«40mm), S. rhombeus
«40mm). GymnotILS
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183
, .. A . 0 N 0Monlll
, M AM" ..Mon."
Fig. 2. Mean monthly standard lengths {or each piscivore species
at Cafio Maraca. Error bars represent one standard deviation
and
coUection sample sizes appear within each open bar.
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184
equal portions of unidentified fish fins and wholeAstyanax
bimaculatus. The largest S. medini speci-mens examined
(71.6-80.6mm) corresponded tosubadult size classes. and all
contained fins (thelargest specimen contained fins and
associatedflesh of Hoplias). Between 40 and 50mm. Pygo-centrus
shifted to a diet comprised primarily ofwhole fishes and sheared
pieces of fish flesh. Awide variety of fish species were taken by
Pygocen-Irus. but primarily Curimata argentea. small omni-vorous
characids. and the large detritivorous char-aciform. Prochilodus
mariae (Prochilodontidae).Adult Pygocentrus consumed portions of
other ver-tebrates (turtles. birds. mammals) when fisheswere
dispersed at low densities during the early wetseason. Hoplias also
shifted to a diet comprised ofdiverse fISh species between 40 and
50 mm. butunlike Pygocentrus. Hoplias always swallowed itsprey
whole. Hoplias is capable of consuming rela-
«I20mm). and Caquetia «40mm. Fig. 3).Ephemeroptera nymphs alone
comprised 65% ofthe diet of juvenile Charax «30mm. Table
I).Gymnotus smaller than 40 mm consumed 62Ofo chi-ronomid larvae
(Diptera). whereas between 120and 240 mm. Ephemeroptera. Odonata
nymphs.and chironomid larvae were predominant in Gym-notus
stomachs. Juvenile Caquetia between 40 and70 mm preyed heavily upon
a wide variety of aquat-ic insects (Table 2).
The shift to a diet comprised primarily of fishcomponents
occurred between 20 and 30 mm for S.irritollS, and between 30 and
40 mm for S. mediniand S. rhombeus (Fig. 3). These
narrow-bodiedpiranhas were fin specialists at subadult and
adultsize classes (Tables 2.3). Fins comprised the majorfraction of
the diet of S. rhombeus larger thanSOmm, although this sample
consisted of only 2specimens. A 195 mm specimen contained
nearly
T~ 1. Resource matrix of dominant rood items consumed by
juvenile size classes or piscivorous fishes at Caito Maraca.
Utilization isexpressed as a percentage of the total volume of the
prey item based on all specimens. Nine fISh and 20 non-fish itenlS
with a combinedvolume of 45.2 liters are not listed (HMA = Hopl;as
molabaricus. CGI - Charax g;bbosus. PNO - Pygocenrrus nolalus. SIR
=Serrasalmus ;rr;lans. SME = Serrasalmus medini. SRH - Serrasalmus
rhombeus. GCA ~ Gymnotus carapo. RHA = Rhamd;a sp..CKR - Caqwlio
trows;;).
HMA 001 PNO SIR SME SRH OCA RHA CKR
o.I.
17O.
I.71.2.
O.I.
I.I.
o.o.O.9.O.o.
37.6.4.4.O.1.1.2.
12.4.
1.
0.170.51
16.30
0.61
5.18
6.01 0.120.619.124.07
-0.24
11.960.072.290.400.020.03
17.~20.120.020.42
0.47O.~1.860.032.15
o.I.I.2.o.
65.4.9.7.O.O.O.
21.O.O.
9.61
O.M
4.50
1.~
1.~
0.0963.89
4.8410.666.92
16.73 20.
O.
1.
O.
2.
-1.04
1.72
5.664.. 1.8 0.49
14.2525.840.41
21.37
4.350.05
3.55
61.-
1.20
Prey category
Vegetative detritus
CopepodaOadocera
AmphipociaEubranchipodaOstracoda
EphemeropteraOdonata nymphsMisc. aq. HemipteraCorixidae
(Hemiptera)
TrichopteraAq. Coleoptera (Iarv)Aq. Coleoptera (adlt)aaironomid
larvae
Mosquito larv.(Diptera)Misc. aq. insectsFish finsMisc. fish
At'qllidt'tUPMCilia
HopliasRachovio
Coq~lia
68.238.635.823.613.887.497.21
4.19
J2B2,10,59
967949
7242
~45
os458S,2S294818388739045368417412
53
202740(1J264003787720a8782(M88
78
21
04
31
4S
-
185
s.lr888tnus thombeua
..-
..~-..-
'.0-
Uo;
u-OA-
u.
M.L:: ~ T - . .'-~~!'0 00 10 '. ,. -
~~(-)
GymnotJ8 ~
'20 '80 200 200 280 320
LengtllrMrval (mm)
. ~fI*IIct8 SII.
fO 80 120
L8ngtI kI-.V8J (mm)
s.r..tInu8lni18ns
.j
!
120.0 80
~ k8V8I (mm).-."'Aq.-.-
~ kt8usU....uuu
~20 .. 80 10 '00 120 '.. '.0L8ngtI ~ (mm)s ~
r ;.~+A4-..-
0.0 ~ ~:2::::::::::::::;?:!':. - : -0 20 40 " 10 100 120 140 ,"
," 200 220 2-0LqfI J..-,y8I (mm)
Fig. 3. Volumetric proportions of microcrustacea. aquatic
insects. and fish prey categories taken by piscivores grouped by
length
interval.
u,u-0.0-
0.2-
0.0-0
-
186
upon small characids, especially Astyanax bimac-ulatus,
Odontostilbe pulcher, and Ctenobrycon spi-lurus. Ctenobrycon
spilurus and Curimata argenteawere the primary prey of large adult
Gymnotus(>200mm). Rhamdia larger than 6Omm con-sumed mostly
whole Curimata, but also fresh re-mains of Astyanax and Prochilodus
that apparentlyresulted from frenzied attacks by schooling
Pygo-centrus. The proportion of fish in stomachs washighly
correlated with standard length (Table 4).
tively large prey items. For example, a 305 mmindividual had
consumed a 95 mm specimen of theheavily armored, spined catfish,
Hoplosternum lit-torale (Callichthyidae). A 288rnrn Hoplias
con-tained a subadult Prochilodus measuring over athird its own
body length. Cannibalism was observ-ed among all size classes of
Hoplias.
Between 50 and 60 mm, Charax shifted fromfeeding primarily on
aquatic insects to small char-acid fishes, particularly
Odontostilbe pulcher. LikeCharax, Caquetia over 70mm preyed most
heavily
Table 2. Partial resource matrix of dominant food items consumed
by subadult size classes of piscivorous fishes at Cano Maraca.
Sevenfish and 28 non-fISh items totalling 43.4 liters are not
listed.
SRH GCA RHA CKRHMA CGI PNO SIR SMEPrey category
o.~
0.020.050.04
6.2510.352.52
14.890.360.450.260.19
0.720.189.59
40.16
7.56
.)"'"-,-
1.263.SJ
0.114.37
0.460.040.570.03
0.11
0.011.050.07
32.516.89
10.3717.19
4.375.S9
---
2".'J'
:;rc~~:
",~
...;'~
M.17
2.41
,..~
::-
.~-,ii,.':;;
! .,.
;~~
j,..;!!'";,
.-
.~
~
.
O.
M).
0
O.
8.
1.
6.
3.
7.
20.
S.
4.
O.
19.
O.
O.
3.
1.
7.
-
c"
...
0.010.21
7.484.760.570.040.10
0.070.26
10.52
3.584.37
3.732.01
25.795.878.313.58
9.67
5.16
.,.~
~~...,..
~:,..
-~~~
~;~J
100
c~;
~~. ~
~;~
-
O.
3.
S.
37.
20.
2.
~.'
1.
-0.011.240.79O.~7.722.022.41
Fine detritus
Aquatic vegetationClams (Mollusca)Oadocera
EubranchipodaShrimp (Decapoda)EphemeropteraOdonata nymphsMisc.
aq. HemipteraCorixidae (Hemiptera)
Aq. Coleoptera (Iarv)Aq. Coleoptera (adlt)Chironomid larvaeMisc.
aq. insects
OnhopteraFish finsMisc. fish fleshMisc. fish (whole)
CorydorasOdonloslilbe
AequidensGephyrocharaxHemigrammusPoeciliaCurimala
AstyanaxHopliosRachoviaT
riportheusMarkianoCaqueliaCheirodontopsGymnotusHypostomusApislogramma
2.382.77
12.630.376.54
15.21
1.164.54
14.221.000.501.001.33
-9.93
-15.68
85
02
,'T7
.40
173S854389541207
0340897999
58999S
10
44OS
4682
,84
93,24
-
187
Tobit' 3. Panial resource matrix of dominant food items consumed
by adult size classes of pisciyorous fishes at Cailo Maraca.
Twentyfour fish and 32 non.fish items totalling 92.9 liters are not
listed.
GCA RHA CKRCGI PNO SIR SME SRHHMAPrey category
5.457.277.271.191.884.353.463.464.15
0.8922.197.006.92
30.63
3.13
2.530.31
-
3.155i.S3
o.
-~~
.!6.
-
e
0.041.910.84
12.01
8.961.240.44S.202.00
3.641.20
26.009.369.88
0.010.15
0.160.260.06
O.OS3.07O.~4.16
20.194.43
25.236.172.24
~.67
0.861.01
12.13
0.4723.1837.13
3.56S.SS0.29
0.920.040.860.13
0.3114.462.220.072.302.34
22.643.747.910.14
S.:M>
S.SS
-2.17O.~
0.17
4.86
16.30
IS.tIJ
2.33
0.05
6.70
2.81
11.38
10.54
0.84
ff~%
~"t~..
76.19
:
n...
Vegetative detritus
Aquatic vegetationHard fruits, seedsFish ewSnails (Mollusca)
Shrimp (Decapoda)Odonata nymphs
OrthopteraArachnidaCtenoid scalesFish finsMisc. fish fleshMisc.
fish (whole)OdontostiJbe
CtenobryconPimelodellaCurimata
AstyanaxProchiJidusRineloricaria
HopliasTriportheusRoeboides
HoplostemumNon-fish vertebrates
50--J7,jS..
;........
I.~
17.17
.,,;:..;::,'""" ..
~~
-
3.10
Table 4. Product moment correlations between the proportion
of fish in the diet and the standard length of piscivores
contain-ing food (0 = P
-
188
... .-OT-DOoro.
c~ I.J0AU0~
8.,
1_1n 1 J 1_- .L _. m~.u t8.PI.Mf"'_U
food ~
Fig. 4. Relative seasonal availability of fish food resources
asindicated by total volumes consumed by the complete CanoMaraca
fish fauna (total volumes recorded in liters for eachseason appear
in the key; AQ = aquatic. TR = terrestrial).
To some degree. seasonal differences in the fre-quency of empty
stomachs were due to ontogeneticdiet shifts. Although no
significant overall effect offish size on frequency of empty
stomachs wasnoted. the largest fishes had significantly moreempty
stomachs than the smallest size class (Table5). The feeding rate of
large piscivores. such as
Hop/ias. often is relatively low due to the timerequired for
digestion of massive prey items priorto the initiation of a new
feeding bout. All of thespecimens of the largest size classes of
the fin-nipping piranhas. S. irritans. S. medini. and S.rhombeus
contained food (Table 5). Pygocentrusand Gymnotus in all three size
classes appeared tobe frequent foragers. To some degree.
frequencyof piscivorous feeding may be overestimated bystomach
contents. because compact bones and stifffin rays are digested more
slowly than soft tissues.Additionally. different digestion rates
for predom-inantly juvenile versus adult prey probably affectsthe
frequency of empty stomachs. Chitinous matterassociated with
invertebrate feeding by smaller pis-civores passes through guts
more slowly than ver-tebrate flesh.
Diet breadth among piscivores showed no signif-icant overall
effect of season (ANOV A). Mean dietbreadth among piscivores was
4.97 during the wetseason. 4.72 during the transition season. and
3.89
Tllblt 5. Percent empty stomachs encountered during three
seasons and within three piscivore size classes.
Species Wet DryTransition Tolal sampl,
HopliasCharax
Pygoct'nlrusS. irrilansS. mt'diniS. rhombt'us
GymnolusRhamdia
Caqut'tia
51.3
31.8
0
4.2
0
3.3
7.4
18.6
.$.1
10.92.86.4004.31.105.5
54.281.8
0
4.829.313.8
389
29S
238
76
68
SO
24M
124
370
13.4Mean 3.4 30.6 F= 3.67.2 DF. P
-
189
50
40
30
20
10HMA CGI ~ SIR SME IRK ~ MIA CKR
SpecIH 0
500.2 0.4 0.8 0.8 1.0 1.2
Fig. 5. Average diet breadths of piscivores during the
wet,transition, and dry seasons at Cano Maraca (HMA =
Hopliasmalabaricus. CGI = Clulrax gibbosus. PNO = Pygocmlrus
no-tatus, SIR = Se"QSalmus irritans, SME = Se"asalmus medini,SRH =
Serrasalmus rlJombeus. GCA = Gymnotus carapo.RHA = RhamdiQ sp., CKR
= Caquffla kraussii).
40
30-020
10
during the peak dry season. The three Se"asa/musspecies
exhibited relatively narrow diet breadths asa result of their
fin-nipping specialization. Dietbreadths showed a trend of lower
values duringdrier periods for Serrasa/mus spp., Hop/ias, Char-ax.
and Rhamdia (Fig. 5). Pygocentrus and Caque-ria exhibited trends of
somewhat more generalizedfeeding during drier periods. Gymnotus was
a moregeneralized feeder during the transition seasonthan either
the wet or dry seasons. During thetransition season, Gymnotus (31-3
mm) took avariety of small fishes and aquatic
invertebrates,especially Odonata nymphs and Hydracarina.Gymnotus
was the principal predator of Ctenobry-con spi/urus, a small
characin that is abundant inthe area throughout the year.
Average seasonal diet overlap among piscivoreswas low (O.I8-wet,
0.19-dry, O.25-transition; Fig.6). For example, the proportions of
cells within thepi/-based overlap matrices with values less than
0.10were 0.53 (wet), 0.57 (transition), and 0.65 (dry).During the
wet season, the largest overlaps werebetween Charax and S. medini
(q> = 1.11,0.46), S.irritans and S. rhombeus (q> = 0.70,
0.60), andGymnotus and Rhamdia (q> = 0.34, 0.74).
Overlaps(Pij-based) equal to or exceeding 1.0 were obtainedfor
Hop/ias x Pygocentrus. Hop/ias x Gymnotus.Hop/ias x Rhamdia, S.
irritans x S. medini. and S.irritans x S. rhombeus during the
transition sea-son. Among 20 pairwise comparisons, only the
Fig. 6. Frequency histograms for piscivore diet overlaps
duringthree seasons at Cano Maraca.
Gymnolus by Rhamdia pairing showed large diet-ary overlap during
the dry season (qJ = 0.64,0.85).
When diet similarities were calculated usingelectivities in
place of Pi!', little diet similarity wasobserved among piscivores
during any season. Theproportions of cells with electivity-based
similar-ities less than 0.10 were as follows: 0.89 (wet),
0.76(transition), and 0.75 (dry). Average seasonal dietsimilarities
were 0.05 (wet), 0.08 (transition), and0.10 (dry). Based on
electivities, the highest dietsimilarity obtained for the wet
season was qJ, = 0.43
-
1~
-..E
g
UN
..
>-U~D-
C.U
~
...2~;Vs.
'0c0
i~L
Fig. 8. Relative proponions of individuals of each species
takenfrom four microhabitat samples during four months of tbe
tran-sition season at Cado Maraca (species codes are the same as
in
Fig. 5).
Spec-Fig. 7. Mean prey sizes encountered in diets or CaJ\o
Maracapiscivor~s during the transition season. Error ban represent
on~standard deviation. th~ number or pr~y items measured
appeanwithin each open bar. and means ror species joined by
linesbelow the x axis were not significantly different at a =
0.05according to Duncan"s Multiple Range Test (species codes arethe
same as in Fig. 5).
(Pygocenlrus x S. rhombeus). Fin specialists, S.irritans x S.
rhombeus provided the only transitionseason similarities exceeding
0.31 (tp, = 0.83, 1.19),whereas Hoplias on Charax (tp, = 0.96)
represent-ed the only pairing above 0.24 during the dry
sea-son.
Prey size
A significant relationship exists between prey sizeand piscivore
species (F = 65.51. 8 OF.P
-
191
Although some opportunity for microhabitat spe-cialization
probably does exist within the turbidwaters of the creek during
these periods (e.g., ben-thic versus midlevel or surface), each
habitat yield-ed rather consistent mixtures of species in
seinehauls.
If one considers three niche axes simultaneously(prey type, prey
size, habitat), and assumes conser-vatively that overlaps greater
than 0.50 are biolog-ically significant, then piscivores separated
on atleast one axis in all but four comparisons during
thetransition season (prey type overlap based on PiJ.Of 36 pairwise
species comparisons, six separatedon all three axes, 18 separated
on two axes, andeight separated on one axis. Of the pairings
thatshow high overlap on all three dimensions, Hop/iasand
Pygocentrus actually had equivocal overlap forhabitat utilization
(cp = 0.32, 0.87), sharing only
open, midpool regions to any large extent. Patternsof foraging
behavior of these species show strikingdifferences as well (i.e.,
solitary, sit-and-wait Ho-p/ias vs. gregarious, pursuit
Pygocentrus). Otherlarge, three-dimensional overlap pairings
corre-sponded to fin-nipping piranha species (S. irri-tans x S.
medini and S. rhombeus; S. medini x S.rhombeus). If
electivity-based diet similaritiesgreater than 0.50 are used as the
criteria for signif-icant dietary overlap, then only the S.
irritans andS. rhombeus pairing showed significant
three-di-mensional overlap during the transition season.
.
HMA CGI PNO SIR SME SRH O.lO)possessed by each piscivore species
during the wet, transition,and dry seasons at CaJ\o Maraca (species
codes are the same asin Fig. 5).
terns such as tropical fish assemblages. Total dietoverlaps were
calculated as the sum of all pairwisediet overlaps exhibited by
niche neighbors duringeach of the three seasons. Two pools of
potentialniche neighbors were analyzed, the nine-speciespiscivore
guild and the entire Cano Maraca fishcommunity. Because not all
species were presentand response to aquatic hypoxia apparently
super-ceded feeding during extended portions of the peakdry season,
only wet and transition season diffuseoverlap trends are
presented.
Analyses of the number of niche neighbors andpatterns of
collective dietary overlap revealed twoclasses of seasonal response
by piscivores. For fivespecies, the number of niche neighbors and
totaldietary overlap were greater during the wet seasonthan the
transition (Fig. 9, 10). Extreme trophicspecialization by subadult
S. medini during thetransition season was indicated by a large drop
intotal diet overlap relative to the previous samplingperiod
dominated by juveniles (CPr = 17.S-wet, 2.7-transition). The
remaining four species (Hop/iDS,Pygocentrus, S. i"itans, S.
rhombeus) had compar-atively few niche neighbors throughout the
year(Fig. 9). Moreover, relatively low total diet overlap(~
-
192
15HopI/.. nl8/.urlcu.
- - 0- - ~Ut«TYaULDCo
~.>0
..'ij
..-0I-
10
0 0
8
T'8n8111on 15We'
10
Q..~.>0.~
.."0I-
0r'8n8ltlonWet
GynwlOlu8 Qrapo
S."...,- /nt,.,.15
A.~~>0
..:;
'i"0I-
T'8naltlon5
~~~~~~048~~~~~~ ~~-~~~~~~-~~..0
TrlnlillenWet
s.n.sa/mus ,ho~s
Do~.>0
i'i
..0I-
TransitionWe'
Fig. 10. Total diet overlap exhibited by each piscivore species
during different seasons at Caiio Maraca. Total community diet
overlaps
are represented by open symbols. and total piscivore guild
overlaps are plotted as closed symbols.
-
193
during the transition season, both within the pisci-vore guild
and the community at large (Fig. 10). Inthe cases of Gymnotus,
Caquetia. and Serrasa/musmedini. collective guild overlaps were low
relativeto overall community overlaps during both the wetand
transition seasons. Rhamdia exhibited a slightincrease in total
guild overlap between the wet andtransition seasons, although
overall communityoverlap declined.
Werner & Hall 1979. Machado-Allison & Garcia1986. Keast
1985b). Morphological changes associ-ated with greater trophic
specialization in the formof piscivory should reduce the efficiency
of mi-croinvertebrate feeding. Following this reasoning.Griffiths
(1975) recognized a dynamic trade-off be-tween maximizing prey
number versus prey energyin the feeding strategies exhibited by
piscivorousyellow perch. Perca flavescens, during ontogeny.
Discussion Resource partitioning
Food resource partitioning was widespread withinthe Cafio Maraca
piscivore guild, particularly dur-ing the transition season. Given
the high concord-ance between ontogenetic diet shifts, prey
avail-ability, and seasonal rainfall, can high levels ofresource
partitioning be interpreted in relation tobiological interactions,
especially interspecificcompetition? Three general, alternative
explana-tions could account for observed patterns of re-source
exploitation. First, resource exploitationcould occur at random.
Yet sufficient subdivisionof available resources was observed among
thenine piscivores as to render this null hypothesisunlikely. For
example, average seasonal diet over-laps were considerably lower
(q> = 0.18 - 0.25)than those obtained for series of randomly
con-structed 100species communities (q> = ca. 0.75,Pianka et al.
1979). Second, contemporary patternsof niche partitioning could be
founded in genetical-ly-based morphological and behavioral traits
thatevolved in response to past environmental condi-tions that
differed from current conditions (sensuConnell 1980). This second
hypothesis contrastssharply with a third possible explanation. that
con-temporary patterns of resource subdivision areadaptive in the
context of present day biotic inter-actions. Interspecific
competition is foremostamong biotic mechanisms cited in studies of
com-munity resource partitioning, although the role ofpredation has
recently received greater attention,particularly with respect to
habitat selection (Fras-er & Cerri 1982, Sib 1982, Werner et
al. 1983,Mittlebach 1984, Power 1984. Power et al. 1985.Hobson
& Chess 1986).
Ontogeny and diet
All nine sympatric, tropical piscivores showed dis-tinct shifts
from invertebrate feeding by small juve-niles to primarily fish
feeding by subadult and adultsize classes. Predominance of fin
nipping by sub-adult and adult size classes of serrasalmine
pira-nhas is consistent with earlier findings (Goulding1980,
Machado & Garcia 1986, Northcote et al.1986, 1987, Sazima &
Zamprogno 1986, Nico &Taphorn 1988). Three primary factors
probably areinvolved in producing size-related patterns of feed-ing
among piscivores. First, juvenile fishes are con-strained by their
small size to exploit relativelysmall food particles (Werner &
Gilliam 1984, Keast1985a, 1985b). Only following a period of
initialgrowth can whole-fish swallowers switch to largerfish prey.
Second, availability of small zooplanktonand benthic invertebrates
(e.g., aquatic insect lar-vae) was much greater during the wet
season com-pared to either the transition or dry seasons atCaiio
Maraca (Fig. 4). Observed switching frominvertebrate to fish prey
largely coincided withchanging food availabilities as indicated by
feedingperformance of the entire fish assemblage. Where-as total
aquatic primary production and aquaticinvertebrate availability
declined during the gradu-al desiccation of the floodplain, fish
densities in-creased markedly. Jackson (1961) made a
similarobservation for African fishes in seasonal aquatichabitats.
Third, many predatory fishes exhibitchanges in relative body
proportions and other an-atomical traits during growth that are
associatedwith greater feeding specialization (Werner 1974,
-
194
In recent reviews of resource partitioning in low-er
vertebrates, Toft (1985) and Ross (1986) in-dicated that causal
factors responsible for differ-ences in resource use are rarely
known. MacNally(1983) and others have argued that descriptive
fieldstudies alone cannot demonstrate competition.Whereas field
experiments potentially can demon-strate interspecific competition
(Schoener 1983),they are beset with problems of interpretation
aswell. Positive, negative, or even a complete lack ofpopulation
response to experimental manipula-tions potentially are confounded
by effects of in-direct interactions (Bender et al. 1984,
Tilman1987) or measurement of inappropriate variables(Diamond 1983,
MacNally 1983). Even though de-scriptive studies cannot demonstrate
competitiondirectly, they often provide strong
circumstantialevidence with the potential to support or reject
thehypothesis of interspecific competition. The infer-ential value
of this circumstantial evidence dependsupon the strength of
comparisons based on inter-population or temporal and spatial
environmentalvariation.
In this study, trophic specializations were associ-ated with
lower diffuse diet overlap during thetransition season when fish
population densitieswere highest and availability of invertebrate
preywas reduced. Due to the general pattern of in-terspecific
synchrony in reproduction with the on-set of the wet season,
ontogenetic shifts towardmore specialized piscivore diets largely
corre-sponded with the progression of the transition sea-son and
fish growth. These observations are consis-tent with McKaye &
Marsh's (1983) hypothesis thatAfrican cichlid fishes switch from
more opportunis-tic, generalized diets to more specialized
feedingduring periods of relative resource scarcity (i.e.,following
the 'niche overlap hypothesis' of Pianka1974). Morphological
adaptations for specializedfeeding may be selectively advantageous
during alimited period during the annual cycle of ecologicalevents.
At Caito Maraca, four species that switchedto piscivory at small
sizes also exhibited low collec-tive diet overlaps throughout the
year (Fig. 10).
In summarizing work involving tropical fish com-munities,
Lowe-McConnell (1987) suggested thatcompetition is potentially most
important during
the late wet and dry seasons in floodplain ecosys-tems. During
this 'crunch period', resources be-come increasingly limited
(especially resources re-lated to space) as local stocks of aquatic
organismsbecome denser within shrinking bodies of water.Biotic
interactions, especially fish predation, in-tensify at this time,
but are piscivores necessarilyresource-limited? Whereas apparent
availability offish prey may be high during the transition
season,niche segregation and trophic specialization amongpiscivores
should OCCl'r for two reasons. First, fol-lowing optimal foraging
theory (Krebs 1978, Pyke1984), scarcity of invertebrate prey and
temporaryabundance of prey fishes would favor exploitationof the
most profitable forms by predators, based ontheir morphology and
innate components of feed-ing behavior. Profitability would be
expressed herein terms of the ratio of energy gained by maximiz-ing
the rate of prey capture, divided by the totalenergy cost
associated with searching, pursuit,handling, digestion, and
assimilation. Evolution-ary divergence of prey escape tactics
increases re-quirements for specialization on a restricted num-ber
of prey species (Rand 1967). Second, the brev-ity of the season of
high fish density, together withthe high risk of mortality due to
predation and dryseason dessication/anoxia, conveys a
tremendousfitness advantage to individuals that maximize
theirintake of temporarily abundant prey, then survivethe ensuing
dry season. A disproportionate frac-tion of the next generation
would be founded byefficient piscivores that are larger and more
fecund(or more effective in providing parental care) thanless
efficient conspecifics. In effect, a major frac-tion of the annual
caloric intake of tIanos piscivoresis concentrated into the
approximately four-monthtransition season. Relative to other
seasons,growth and visceral fat deposition is maximal formost
species during the transition season (personal
observation).Given the selective premium that is placed on
highly efficient foraging by subadult and adult pis-civores
during the transition season, it appears like-ly that observed
trophic specializations are adap-tive in reducing the negative
impact of diffuse com-petition within this rich fish assemblage.
For com-petition to occur, resources must be in limited~
-
195
mass in stomach contents was estimated fromlength/mass
relationships. Both of these factors in-crease risks of sampling
error. Third, and mostseriously, the taxonomic identities of the
eight fishspecies are confused (see Taphorn & Lilyestrom1985
for listing of regional ichthyofauna). The onlyunconfused species
name, Roeboides dayi (Stein-dachner), is perhaps the most suspect
of the eight.Prejs & Prejs (1987) found 99.9 and 100%
vegeta-tion and detritus in the stomachs of R. dayi duringthe dry
season, whereas fish scales comprised 76(N = 121) and 25% (N = 49)
of the diet of R. dayiat Calio Maraca during the transition and dry
sea-sons respectively. Scales formed 24 (wet) and 15%(dry) of the
diet of R. dayi by volume at CalioVolcan, a small piedmont stream
(N = 313, Wine-miller 1987a). All other Roeboides species, forwhich
data are available, specialize on scales inaddition to aquatic
insects (Sazima 1983, Wine-miller 1987a). Most of the fishes
referred to as 'R.dayi' by Prejs & Prejs (1987) were probably
Cre-nobrycon spilurus (Valenciennes), a morpholog-ically similar,
omnivorous characid that is extreme-ly common in shallow,
productive environmentsthroughout the llanos.
Some temperate zone studies also have demon-strated greater diet
segregation among fishes dur-ing periods of reduced food
availability (Nilsson1955, Harrington & Harrington 1961,
Thorman1982). In addition to diet segregation, interspecificsize
and time related differences in habitat use havebeen demonstrated
for both temperate and tropicalfish assemblages (Werner & Hall
1977, Moyle &Senanayake 1984, and see Ross 1986 for
others).Habitat segregation by Calio Maraca piscivoresprobably was
as much a function of predator avoid-ance as food resource
segregation. Fishes used aq-uatic vegetation as the principal form
of cover foravoidance of predation by dense schools of red-bellied
piranhas, Pygocentrus noralus. Additional-Iy, and perhaps to a
lesser extent, smaller fin-nip-ping Serrasalmus species posed a
threat to diurnal,open-water dwellers. Where it is common,
Pygo-centrus may have a pervasive effect on the spatialstructuring
of fish communities, since only highlycryptic, heavily armored, or
fast schooling fisheswere generally taken from deep open-water
re-
supply and contested by two or more populations.The presence of
numerous heterospecific pisci-vores during the transition season of
high fish den-sity could restrict foraging to the most
profitableprey types. Reductions in pairwise diet overlapduring
periods of reduced food availability havebeen shown in several
earlier studies of fish com-munities (see Ross 1986). Though based
on limitedsampling, reduced diet overlap among fishes wasreported
by Zaret & Rand (1971) and Greenfield etal. (1983) during the
dry season in Central Amer-ican streams. Alternatively,
lowe-McConnell(1964), Knoppel (1970), and Goulding (1980)stressed
high dietary overlap in South Americanfish communities, although no
attempts were madeto study trophic guilds quantitatively over
time.The findings of the current study contrast sharplywith those
of Knoppel (1970), who interpreted hisdata as indicating a
perplexing lack of correspond-ence between morphological
characteristics anddiets of fishes from five stream collections in
cen-tral Amazonia. Also in opposition to the currentfindings was
Knoppel's (p. 346) contention that'stomach contents according to
age of fishes did notmerit close consideration'. Quite the
contrary,Knoppel probably did not examine stomachs andsize classes
closely enough to discern the obvious
patterns.Recently, Prejs & Prejs (1987) observed higher
dietary overlap during the dry season among
small,vegetation-dwelling fishes in seasonal pools of theVenezuelan
low llanos. These authors interpretedpatterns of diet overlap as
ecologically unimpor-tant, because their data showed reduced
feedingrates or a switch to detritivory during the dry sea-son
(apparently, the dynamic transition season ofthe llanos was not
sampled). Lower availability ofinsect prey and increased predation
pressure werebelieved to be the primary factors accounting
forreduced dry season feeding; however, results ob-tained by Prejs
& Prejs (1987) must be interpretedwith caution for several
reasons. First, their com-munity subset of eight small,
vegetation-dwellingfishes does not represent a trophic guild, but
rathera diverse subset of small vegetation-dwelling fish-es.
Secondly, total sample sizes for stomach con-tent analysis were
small (N = 9-30), and prey bio-
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196
the Mato Grosso region of western Brazil (I. Sazi-ma, personal
communication). Further field andlaboratory studies are needed to
sort out the nicherelations of fin-nipping piranhas more
accurately.
Conclusions
High fish species diversity in the neotropics is asso-ciated
with impressive morphological and ecolog-ical diversification
(Roberts 1972, Fink & Fink1979, Goulding 1980, Sazima 1986,
Lowe-McCon-nell 1987). Coexistence of more than 100 fish spe-cies
in some llanos creeks (Taphorn & Lilyestrom1985) may be due in
part to relaxed interspecificcompetition during horizontal flooding
and thebloom of primary production that occurs during thewet
season. Diets of five of the nine piscivoresexamined overlapped
more with the rest of the fishcommunity during this period than any
other.Large diffuse overlap during the wet season largelyresulted
from heavy exploitation of abundant mi-crocrustacea and aquatic
insect larvae by juveniles.Lower collective overlap during the
transition sea-son probably was derived from complex interac-tions
among several factors, including: (1) reducedavailability of
juvenile food resources, (2) fishgrowth and ecomorphological
trade-offs favoringdiet shifts, (3) increased fish densities and
diffusecompetition favoring maximal rates of prey exploi-tation,
(4) differential prey profitability due totrade-offs associated
with prey escape tactics, and(5) the threat of predation by
piranhas restrictingdiurnal foraging by other piscivores in
open-watermicrohabitats. In highly diverse communities, dif-fuse
overlap with numerous niche neighbors repre-sents a greater
potential negative effect than isolat-ed pairwise interactions.
gions of Cano Maraca and other ilanos streamsduring daylight.
Nocturnal predators (e.g. Rham-dia and Gymnotw) leave the dense
mats of aquaticvegetation to forage in the open water habitat
un-der cover of darkness. Approximately 80 man-hours of nocturnal
hook-and-line fishing at astream in the low llanos of Apure state
(location ofCano Maporal given in Nico & Taphorn 1988)yielded
nine species of large piscivores (unpublish-ed data). Diurnal
hook-and-line fishing over thesame period yielded 13 large
piscivorous species,yet only three species occurred in both
samples(e.g. Pygocentrus notatus, Pseudoplalystoma las-ciatus, and
Plagioscion squamosissimw). Sixty sev-en percent of the nocturnal
sample was comprisedof siluriforms (catfishes and knifefishes),
whereas92% of the diurnal sample belonged to the
ordersCharaciformes (piranhas, tetras, and relatedforms) and
Perciformes (cichlids and one fresh-water drum). Furthermore, most
diurnal piscivoreswere taken near cover at the stream margin,
fur.ther supporting the hypothesis that Pygocentrusrestricts
diurnal use of the open-water, midpoolhabitat by other
piscivores.
The three fin-nipping piranhas exhibited thehighest similarities
in diet and habitat niche para-meters at Cano Maraca. As might be
expected dueto genetic and morphological similarities,
closelyrelated species frequently exhibit relatively lessecological
segregation than more distant taxa.Lack of diet segregation among
fin-nipping pira-nhas, especially Serrasalmw irritans and S.
rhom-beus subadults, was due in part to my inability toidentify fin
fragments at the species level in mostinstances. Records of the
incidence of fin nips onpreserved Cano Maraca specimens clearly
indicatethat not all fishes are equally vulnerable to Serra-salmw
attacks (unpublished data). Preliminarytests of aquarium-housed
juveniles and subadultssuggest that Serrasalmw species possess
distinctpatterns of foraging behavior associated with eitherstealth
in open water (S. irritans; see Nico & Ta-phorn 1988 for a
brief description of field observa-tion), persistent chasing with
frequent remaneu-vering (S. medini), or use of cover for
ambushing(S. rhombew). Similar behavioral patterns wereobserved
among three syntopic piranha species in
Acknowledgements
I thank D.C. Taphom for his support and hospital-ity in
Venezuela. The field assistance of D.C. Ta-phom, L. Nico, A.
Barbarino, and N. Greig wasgreatly appreciated. I thank P. Urriola,
R. Schar-gel, F. Mago-Leccia, and C. Hubbs for assistance
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197
in obtaining permits and visas. The Direcci6n Ad-ministracion y
Desarrollo Pesquero of the Repub-lic of Venezuela provided a
collecting permit. I amgrateful to D. Urriola for kindly allowing
me towork on his property. This study was derived froma doctoral
dissertation submitted to the Depart-ment of Zoology of the
University of Texas inpartial fulfillment of the requirements for
thePh.D. I thank my advisors E.R. Pianka and C.Hubbs for their
support. Funds were provided by aresearch grant from the National
Geographic So-ciety and an NSF predoctoral research grant.
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