The Ecology of Coral Reef Fishes
Modified in May 2003 for QUEST
by Leon E. Hallacher
University of Hawaii at Hilo
Introduction
One of the first things that catches the attention of a diver entering the warm
waters of the coral reef is the phenomenal diversity, abundance, and beauty of fishes
swimming before them. While all organisms on the coral reef are integrated into its
overall ecology, fishes are certainly among the more readily observable taxons, and are
an extremely important component of overall reef function. No comprehensive survey
or community-level study of a coral reef would be complete without fishes being
evaluated. Because of their importance, which is reflected by the large volume of
literature on their biology, this chapter is devoted entirely to the ecology of coral reef
fishes.
Before proceeding further, it seems appropriate that at least a basic introduction
to fishes be provided for students who have not had courses in general zoology or
introductory ichthyology. First, what is a fish? While that might seem intuitively
obvious, the shear evolutionary diversity of fishes, makes defining them somewhat
problematical. Nonetheless, a workable definition comes from Nelson (1984) who
states, "...fish can be simply defined as aquatic poikilotherm vertebrates that have gills
throughout life and limbs, if any, in the shape of fins."
Of vertebrates, fishes account for about half of the approximately 43,000 living
species. There are currently about 21,723 living fish species, comprising roughly 445
families placed in 50 orders (Nelson 1984). Of the 21,723 species of fishes, about 58%
are marine, 41% live in freshwater, and the remainder (1%) migrate regularly between
marine and freshwaters (Cohen 1970).
At the highest taxonomic level of differentiation, living fishes are subdivided into
four classes:
Approximate
Class
Common Name
Number of Species1
Cephalaspidomorphi
Myxini
Chondrichthyes
Osteichthyes
1
lampreys
hagfishes
cartilaginous fishes
bony fishes
From data provided by Nelson (1984).
1
41
32
793
20857
The lampreys and hagfishes are living remnants of a much more speciose
assemblage of jawless fishes called ostracoderms that flourished in the seas during the
Silurian and part of the Devonian (roughly 400-300 million years before the present).
These eel-like fishes lack jaws, paired fins, bone, and vertebral column, although they
do have a persistent notochord (Nelson 1984). Unlike other fishes, their gills open
externally via numerous pores. Lampreys are found in the cold fresh and/or marine
waters of higher latitudes, and are most notorious for parasitizing other fishes by
sucking their bodily fluids. Hagfishes are found in marine waters less that 13o C, which
confines them to temperate seas or to the deep (and cold) bottom of tropical oceans.
They occupy soft bottom regions where they forage for small infaunal invertebrates or
scavenge on dead organisms.
Fishes of the class Chondrichthyes possess cartilaginous skeletons although
teeth, jaws, and vertebral column can be calcified. Other chondrichthyian features
include: a skull which lacks sutures; unsegmented soft fin rays; swimbladder or lungs
absent; and internal fertilization (Nelson 1984). The class includes the sharks, skates,
rays, chimaeras and ratfishes, and is subdivided into six or 13 orders depending upon
the author (Nelson 1984 or Compagno 1973, 1977). Distributed world wide,
cartilaginous fishes are all carnivorous although feeding habits are diverse, ranging from
planktivores to benthonic mollusc/crustacean crushers, to predators that bite large
chunks of flesh from their prey. While many species are associated with coral reefs,
their behavior and ecology has generally received less attention from investigators than
that of bony fishes. This is probably mostly the result of the difficulty associated with
studying large mobile fishes like sharks, rays, and skates. Certainly it is not due to any
lack of interest from scientists toward the chondrichthyian fishes. Nonetheless, much
less is known about them as a group compared to the bony fishes and they will not be
treated further in this chapter.
The class Osteichthyes is comprised of fishes which have skeletons, at least in
part, with true bone. The group also possesses numerous other features including: a
skull with sutures; segmented soft fin rays; a swimbladder or functional lung which is
usually, but not always, present; and a preponderance of species utilizing external
rather than internal fertilization (Nelson, 1984). The Osteichthyes contains
approximately 20,857 species of bony fishes that split into at least four evolutionary
lines early in their evolution (Moyle and Cech 1988, Nelson 1984). Those lines are: 1)
the lungfishes represented today by six freshwater species living in Africa, South
America, and Australia; 2) the crossopterygians represented by a single remaining
species, the coelacanth, inhabiting the deep marine waters off eastern Africa; 3) the
bichirs, eleven freshwater species found in central Africa; and 4) the ray-finned fishes
represented by the remaining 20,839 species of bony fishes.
The ray-finned fishes include sturgeon and paddlefishes (25 species), gars (7
2
species), bowfin (1 species), and teleosts (20,806 species). Teleosts, which comprise
99.8% of all bony fish species, are commonly referred to as "advanced" bony fishes.
The group contains 35 orders which exhibit remarkable diversity of form and life-style.
Nonetheless, the advanced bony fish fauna is dominated by the fishes of a single
teleost order, the Perciformes. One hundred and fifty of the 445 families listed by
Nelson (1984) are contained within the order Perciformes, and some of those 150 are
the most speciose of fish families [i.e. gobies (Gobiidae) - about 1500 species, wrasses
(Labridae) - about 500 species, sea basses (Serranidae) - 370 species, etc.]. Species
from this order are the dominant component of coral reef fish fauna.
As might be expected, fishes are not uniformly distributed throughout the world's
oceans. About 9800 marine species (78% of all marine species) live along margins of
land masses in waters to about 200 m deep (Moyle and Cech 1988). Somewhere
between 66-89% of those 9800 species (30-40% of all fish species) are found on coral
reefs and associated habitats around the world (Moyle and Cech 1988)! Without
question, coral reefs have by far the highest diversity of ichthyofauna of any marine or
freshwater ecosystem.
Given the diversity of coral reef fishes, high variability between coral reef fish
communities world-wide, and the voluminous literature on the ecology of coral reef
fishes, it is beyond the scope of this chapter to even begin to fully treat the subject of
the biology and ecology of coral reef fishes. While this narrative provides good general
coverage of several important topics relating to the biology of coral reef fishes, it
necessarily lacks depth. For the student who wishes to pursue the subject in greater
detail, an excellent review of coral reef fish ecology is available (Sale 1991a).
Evolution of Coral Reef Fishes
Where did coral reef fishes come from and when did they evolve? For the most
part, to talk about the evolution of coral reef fishes is to talk about the evolution of
perciform fishes since the vast majority of reef fishes are from this order. According to
Carroll (1987) the perciforms arose from beryciform-like acanthopterygian (spiny-rayed)
ancestors during the late Cretaceous some 65-70 million years ago (modern beryciform
fishes include familiar fishes like squirrelfishes, soldierfishes, and beardfishes).
Between the late Cretaceous and the early Tertiary (to about 50 million years before the
present), the perciform fishes underwent a period of rapid evolutionary change (Carroll
1987). Within about 20 million years of the first appearance of perciform fishes, they
achieved a structural complexity and taxonomic diversity that is essentially
indistinguishable from that of living forms (Choat and Bellwood 1991).
The appearance and subsequent rapid evolution of perciform fishes coincides
closely with changes in coral reefs that were occurring at approximately the same time
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(Rosen 1988, Choat and Bellwood 1991). While reef-building corals were present long
before the late Cretaceous, they were not the scleractinian corals that dominate modern
reefs. Scleractinians did not appear in the fossil record until the late Cretaceous/early
Tertiary, after a period of decline and extinctions of many earlier coral taxa at the end of
the Cretaceous (Fagerstrom 1987). In the early Tertiary, scleractinian corals became
the dominant coral taxa and coral reefs, which were predominant features of many
shallow tropical seas, took on a modern appearance (Choat and Bellwood 1991). In
summary, modern coral reef fishes are an ancient group which evolved some 70-50
million years before the present in conjunction with the evolution of modern coral reefs
dominated by scleractinian corals. As such, the biology of both reef corals and fishes is
intimately intertwined.
Coral Reef Fishes - Taxa of Major Importance
Approximately 100 families of bony fishes are known to have coral reef
representatives (Leis 1991a). Of those, perciform fishes predominate in regard to both
species richness and abundance. Of 103 families of reef fishes cataloged from reefs in
Micronesia, 51 were perciforms (Myers 1989, Choat and Bellwood 1991). Williams and
Hatcher (1983) in their survey of reef fishes from various habitats on the Great Barrier
Reef found that perciform fishes were by far the most abundant on the reefs sampled
Of the 50 or so perciform families associated with coral reefs, just eight families
from three major taxa are particularly important in regard to complete association with
coral reef environments (Choat and Bellwood 1991, Sale 1991b):
Labroids
Labridae Scaridae Pomacentridae -
wrasses
parrotfishes
damselfishes
Acanthuroids
Acanthuridae Siganidae Zanclidae -
surgeonfishes
rabbitfishes
moorish idols
Chaetodontoids
Chaetodontidae Pomacanthidae -
butterflyfishes
angelfishes
The vast majority of these fishes have distribution patterns which correspond to
the distribution of coral reefs and spend their entire postsettlement life cycle in
association with those reefs (only a small percentage of the labroids have invaded
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colder waters of temperate reefs). Within all of these taxonomic groupings there is a
tendency for ecologically similar species to form extensive guilds, which in itself, is one
of the distinctive elements of coral reef fish faunas (Choat and Bellwood 1991). The
fishes of these groupings also have feeding habits which have diverged dramatically
from the generalized large-mouthed carnivores from which they evolved. Many are
"picker-type" microcarnivores or herbivores which exploit the benthonic biota of coral
reefs, while others have adopted planktivory as their primary mode of feeding.
The labroids include the wrasses, the parrotfishes, and the damselfishes.
Wrasses are a large family of some 500 carnivorous species which specialize in taking
benthonic invertebrates, primarily crustaceans and molluscs (Sano et at 1984). There
are about 68 species of parrotfishes and most are primarily herbivorous. The
damselfishes, which total 235 species worldwide, have diets which range from
herbivory, to planktivory, to feeding on benthic crustaceans. Many wrasses and
parrotfishes exhibit sequential hermaphroditism and have complex social systems.
Territorial behavior is common among the damselfishes.
The acanthuroids include the surgeonfishes, rabbitfishes, and moorish idols.
There are about 76 surgeonfish species, 25 rabbitfish species, and only one species of
moorish idol (included in the surgeonfish family by Nelson 1984). For the most part,
fishes of these families are herbivores or detritivores, although some of the
surgeonfishes, especially species from the genera Naso and Acanthurus, are
planktivores (Choat and Bellwood 1991). Although not as speciose as the labroids and
chaetodontoids, their largely herbivorous feeding behavior has profound impact on the
ecology of coral reefs, and acanthuroids are often among the most abundant fishes on
coral reefs (Choat 1991).
The chaetodontoids include the butterflyfishes and the angelfishes. Both families
exhibit marked lateral compression, possess small terminal mouths with bristlelike teeth,
and are often among the most brightly colored fishes on the reef. There are some 114
species of butterflyfishes, of which 90% occur in the Indo-Pacific (Allen 1981). Almost
half of the butterflyfishes feed on corals, although others feed on small reef
invertebrates, algae, or even plankton. There are 74 species of angelfishes, most
occurring in the western Pacific (Choat and Bellwood 1991). Angelfishes exhibit three
main feeding strategies: consumption of benthonic invertebrates (mainly sponges),
herbivory, and plankton feeding (Allen 1981).
Sale (1991b) also points out that there are at least eleven additional families of
fishes that can be considered especially important based on a combination of reef
association and study by marine ecologists. Those families include: the speciose
demersal, site attached blennies (Blenniidae) and gobies (Gobiidae); the small,
nocturnally active predatory cardinalfish (Apogonidae) and grunt (Haemulidae) families;
the bizarre and highly evolved boxfishes (Ostraciidae), puffers (Tetraodontidae), and
5
triggerfishes (Balistidae); the large, often piscivorous, predatory sea basses
(Serranidae), snappers (Lutjanidae), and emperors (Lethrinidae); and the frequentlyplanktivorus squirrelfishes and soldierfishes (Holocentridae).
Coral Reef Fishes - Zoogeographical Considerations
The zoogeography of marine fishes is much less well understood in comparison
to that of their freshwater counterparts which exhibit patterns of distribution based
largely on continental drift (plate tectonics) and the geography of drainage systems.
Zoogeographical regions of marine fishes have generally been defined on the basis of
fish faunal changes, which themselves seem to correlate to changes in oceanographic
conditions relating to current patterns or geographic location. Because of the mobile
nature of fishes and the widespread pelagic dispersal of marine fish larvae,
zoogeographic boundaries are not clear-cut nor are they rigid in time (Moyle and Cech
1988). As a result, discussions of the zoogeography of marine fishes have been largely
descriptive in nature.
An exhaustive, relatively recent, and widely cited treatment of the subject of
marine zoogeography is the work of Briggs (1974). Briggs divided tropical oceans into
four large regions, based primarily on the distribution of reef fishes. Those regions are:
1) the Indo-Pacific Region, 2) the Eastern Pacific Region, 3) the Western Atlantic
Region, and 4) the Eastern Atlantic Region. These regions are separated from each
other by continental land masses or vast expanses of deep ocean, and possess
northern and southern boundaries which correspond roughly to the 20o C isotherm for
the coldest period of the year (Moyle and Cech 1988).
The Indo-Pacific region is by far the largest of Briggs' zoogeographical regions
stretching from the east coast of Africa all the way to the Hawaiian Islands, Marquesas,
and Easter Island. This region is rich in coral reefs and easily has the highest diversity
of reef fishes of any of Briggs' regions. There are probably in excess of 3000 species of
shore fishes in the Indo-Pacific, compared to less than 1000 for each of the other
regions (Briggs 1974). Many of these 3000+ species are wide-ranging over vast
distances within the Indo-Pacific. However, isolated oceanic island chains in the IndoPacific region often have a rich endemic fauna. For example, in Hawaii about 30% of
the reef fish fauna is endemic, the highest level of endemism for marine fishes in the
Indo-Pacific region (Hourigan and Reese, 1987). While most families of coral reef
fishes occur in all four of the regions, a few families are endemic to the Indo-Pacific like
pegasids (seamoths), sillaginids (smelt-whitings), kraemeriids (sand gobies), siganids
(rabbitfishes), and plesiopids (roundheads) (Moyle and Cech 1988). Although the IndoPacific region shares most of its fish families with other regions, only a small number of
species occur in other zoogeographical regions: sixty-two species are shared with the
Eastern Pacific, eight species with the Western Atlantic, and 32 species with the
6
Eastern Atlantic (Moyle and Cech 1988).
The Eastern Pacific Region extends along the west coast of the New World from
the tip of Baja California to the Gulf of Guayquil which lies at approximately 3o south
latitude on the west coast of South America. It is separated from the Indo-Pacific by
expanses of deep ocean and from the Western Atlantic by the isthmus of Panama and
contains some 800+ species of shore fishes (Moyle and Cech 1988). The Western
Atlantic Region, home to over 900 species of near shore fishes, includes the eastern
coastlines of Mexico and Central America, the east coast of South America to Cape
Frio, the tip of Florida, and numerous islands of the West Indies and Bermuda (Moyle
and Cech 1988). Coral reefs are well developed in the Western Atlantic Region and
much of its fish fauna is associated with those reefs. While ecological roles of fishes on
these reefs appear to be similar to those on Indo-Pacific reefs, only eight species are
shared by the two regions, and subtle differences in the ecology of their fishes exist.
For example, in the Indo-Pacific the principal cleaner fishes are wrasses while in the
Western Atlantic, that ecological role is assumed by the gobies (Moyle and Cech 1988).
The Eastern Atlantic Region, the smallest and most isolated of the four regions defined
by Briggs, extends along the west coast of Africa from Cape Verde to Angola and
includes the offshore islands of Cape Verde, St. Helena, and Ascension. This is the
most species-poor region, possessing only about 450 species of shore fish. It contains
few coral reefs which may help to explain its relatively low richness of fish species.
Reflecting the region's relative isolation, about 40% of the fish species are endemic
(Moyle and Cech 1988).
In a recent paper, Thresher (1991) reviewed and evaluated literature on
geographic variability in the ecology of coral reef fishes. His review includes an
evaluation of geographic trends in species and family richness which is relevant to this
discussion of coral reef fish zoogeography. Working from species checklists compiled
by other workers from twenty-one different warm-water locations in the Indian, Pacific,
and Atlantic Oceans, Thresher plotted the number of species and families present at
each location against the location's longitude within its respective ocean basin.
For sites within the Pacific Ocean, Thresher found that there was a statistically
significant decline in the number of species and families from west to east across the
basin. Indian Ocean sites exhibited an opposite, though nonsignificant, trend (an
increase from west to east). The observed longitudinal gradients in species and family
richness within the Indo-Pacific seem to correlate well with the widely accepted
hypothesis that the center of coral reef fish diversity (radiation) is the Philippines-IndoMalayan region.
In fact, out of the sites analyzed, Thresher found the highest number of species
(about 1000) and families (about 50) from reefs located near the western continental
margin of the Pacific (Guam, Great Barrier Reef, New Caledonia). New World reefs
7
(Sea of Cortez, Florida Keys, and the Bahamas) and isolated islands in the Pacific
(Tahiti, Johnston Island, Hawaiian Islands, Easter Island, and the Galapagos) and
Atlantic (Ascension Island) are inhabited by far fewer species (about 60-80% less) and
families (about 12-30% less) than the species and family rich western Pacific region.
Hawaiian reef fish fauna were recently evaluated by Hourigan and Reese (1987)
who identified four main evolutionary/zoogeographical characteristics of Hawaiian
fishes. First, they share a close affinity with Indo-west Pacific (IWP) fishes. Most fish
species found in Hawaii also occur in the IWP (approximately 70%), and most Hawaiian
endemics have sibling species in the IWP. Second, the species richness of Hawaiian
fishes, and reef fauna in general, is depauperate relative to their IWP counterparts. In
the Philippines, located near the center of IWP fish radiation, there may be as many as
2000 species of fishes. Hawaii only has about 680 species; 440 inshore and 240
epipelagic and deeper. Other Hawaiian marine taxa exhibit similarly low species
richness: 2500 IWP mollusc species vs 1000 Hawaiian species; 354 IWP echinoderms
vs 90 in Hawaii; >53 IWP coral genera vs 15 Hawaiian genera; etc.. Third, Hawaiian
reef fishes exhibit the highest degree of endemism at the species level (about 30%
endemics) in the IWP region (for marine fauna). Endemism is also high among other
Hawaiian marine groups; 18% for algae, 20% for molluscs, 20% for asteroids, and 40%
for polychaetes. Fourth, there is a lack of adaptive radiation among the fishes of the
Hawaiian Island chain. Most species are found on all islands and there appears to be
high genetic similarity from island to island.
Hourigan and Reese (1987) explain the observed characteristics on the basis of
an interaction between Hawaii's geographic isolation and the life-history of most coral
reef fishes. The vast majority of marine organisms, including fishes, produce floating
eggs or larvae which are dispersed by water currents (reproduction in coral reef fishes
will be discussed in more detail in the next section). Once young recruit to a reef,
individuals generally remain near where they settle for the balance of their lives.
According to Hourigan and Reese, the low species richness which characterizes
Hawaiian reef fishes is reflective of how difficult it is for organisms with this life-history
pattern to reach Hawaii. Adults, which technically might be able to swim to Hawaii from
other areas (probably the Indo-west Pacific), aren't inclined to attempt such migrations.
Eggs or larvae of reef fishes are rarely in the water for more than about 80 days (often
far less). This is not nearly long enough for them to reach the remote islands of the
Hawaiian chain, which do not have any direct current systems leading to them from the
IWP or elsewhere.
Hourigan and Reese also point out that Hawaii's isolation probably also accounts
for its pronounced endemism. Once species do somehow make it to Hawaii (one
mechanism, for example, might be by rafting under floating marine debris), they are well
8
isolated from their parental stock. Little or no gene flow occurs so divergence and
ultimately speciation become more likely. However, island-to-island radiation
(speciation) has not happened because planktonic larval dispersal does allow gene flow
to occur among fish populations within the Hawaiian Island chain. There is therefore
less chance for inter-island divergence, and ultimately speciation, to occur.
Features of the Life History of Coral Reef Fishes
The life-cycle of most coral reef fishes can be subdivided into three distinct
biological/ecological phases: 1) a pelagic larval phase, 2) a juvenile phase, and 3) an
adult phase. During the pelagic phase, eggs and/or larvae float in open water as a
component of marine plankton. The juvenile phase begins when the young fishes settle
onto the reef in a process referred to as recruitment. Juveniles tend to be secretive and
are less likely to be seen than adults. The adult phase is marked by the onset of sexual
maturity, and may be accompanied by a transition from juvenile to adult coloration or
morphology. For the majority of coral reef fishes, it is the adult phase which has
received the most attention, and only relatively recently has the importance of larval,
and to a lesser extent juvenile, ecology been recognized (Doherty 1991, Jones 1991,
Leis 1991a, Richards 1982, McFarland 1985, Richards and Lindeman 1987).
Although marine bony fishes are taxonomically and ecologically diverse, the
overwhelmingly majority of species have life-histories which include a pelagic larval
stage. Leis (1991a) summarized reproductive characteristics of 100 families of bony
fishes associated with coral reefs. Out of the 100 evaluated, only four families had lifecycles with no pelagic stage (Plotosidae-eeltail catfishes, Batrachoididae-toadfishes,
Pholidichthyidae-the convict blenny, and Sciaenidae-drums/croakers). Leis also noted
that one damselfish species, Acanthochromis polyacanthus, was reported to lack a
pelagic larval stage (Robertson 1973).
Thresher (1991) recognized the two most common spawning modes for coral
reef fishes as being: 1) pelagic spawning in which buoyant eggs are shed directly into
the water column where they disperse and ultimately hatch into larvae; and 2) demersal
spawning in which negatively-buoyant adhesive eggs are tended (usually) by one or
both parents until they hatch into larvae which then undergo a planktonic phase. In
addition, some coral reef fishes brood their eggs orally or in body pouches, are livebearers, or produce semi-pelagic eggs with tendrils that may attach them to objects or
join them in free-floating clumps (Leis 1991a, Hourigan and Reese 1987, Nelson 1984,
Moyle and Cech 1988). The life cycles of coral reef fishes are summarized in Figure
F1.
The pelagic larval stage predominates regardless of the spawning mode. Of the
9
96 families of coral reef fishes listed by Leis (1991a) with a pelagic larval phase, 57
were pelagic spawners (i.e. wrasses, parrotfishes, surgeonfishes, snappers, goatfishes,
butterflyfishes, moray eels, etc.), 14 were demersal spawners (i.e. damselfishes,
triggerfishes, gobies, blennies, puffers, etc.), two were live-bearers (viviparous brotulas
and clinids), six were brooders (ghost pipefishes, and pipefishes and seahorses in body
pouches; mouthbrooding cardinalfishes, jawfishes, basslets, and sand stargazers),
three produced semi-pelagic eggs (halfbeaks, needlefishes, and silversides), four
exhibited more than one type of reproductive mode (herrings, frogfishes, roundheads,
and labrisomids) and 10 have an unknown reproductive mode.
The study of pelagic larvae is difficult for several reasons. First, there are the
obvious logistic problems associated with accessing and collecting planktonic fish larvae
far from shore. Second, the pelagic larvae of reef fishes are difficult to identify to
species or even genus for several reasons (Leis 1991a). They are usually very small
which makes them difficult to work with. They are not fully developed at hatching and
hence pass through many different developmental stages prior to settlement. They
often have morphological features as larvae, like fin or cranial spines exceeding the
total head-to-tail length of the larva, which are lost when they recruit to the reef.
In spite of these difficulties, information is becoming increasingly available on the
natural history and ecology of pelagic reef fish larvae. The length of time that larvae
spend as constituents of the plankton is dependent upon species and probably highly
variable within each species (Leis 1991a). Furthermore, the length of the pelagic stage
may vary geographically or seasonally (Randall 1961, Victor 1986a). Hourigan and
Reese (1987) compiled estimates of larval duration for nine families of Indo-west Pacific
reef fishes based on analyses of daily growth increments on otoliths by other workers
(Brothers et al 1983, Brothers and Thresher 1985). Means ranged from a maximum of
about 75 days for the pelagic spawning moray eels to a minimum of 20 days for the
mouth-brooding cardinal fishes. The pelagic phase probably ranges from 9 to well in
excess of 100 days (Leis 1991a; Brothers and Thresher 1985; Victor 1991, 1986a,b,
1987; Thresher et al. 1989), while the majority of reef fishes appear to have pelagic
larval dispersal times of 20-30 days (Victor 1991).
During the pelagic phase, most tropical shorefish larvae appear to feed on other
zooplankton including copepods, tintinnids, nauplii, mollusc larvae, larvaceans,
chaetognaths, rotifers, and other fish larvae (Randall 1961, Watson 1974, Liew 1983,
Jenkins et al. 1984, Houde and Lovdal 1984, Schmitt 1986, Finucane et al. 1991, Leis
1991a). The data available suggest that tropical shorefish larvae have high dietary
specificity and that the arrays of items consumed shift with ontogenetic change (Leis
1991a). Most larvae appear to feed mostly during daylight hours, although some may
feed more at night (Leis 1991a). Existing data do not support the hypothesis that
starvation is a major cause of mortality of reef fish larvae in the purportedly "foodscarce" waters of tropical seas (Doherty et al 1985). A high percent of larvae examined
10
in feeding studies have food items in their gut, although as Leis (1991a) points out, it is
possible that starving larvae may disappear quickly as a result of increased predation.
The pelagic larvae of reef fishes are by no means homogeneously distributed
throughout their range, but instead exhibit pronounced heterogeneity both horizontally
and vertically. Gray (1993) collected larval fishes along a series of transects running
perpendicular to shore between the 30 m and 100 m depth contours off central New
South Wales, Australia. Collections were made at the surface and at 20-30 m of depth
at three locations along each transect (over the 30, 70, and 100 m depth contours). He
found heterogeneity to exist in the horizontal and vertical distributions of many taxa, with
horizontal distributional differences being apparent in the inshore-offshore direction (i.e.
correlated to bottom depth) rather than longshore. Of 35 families evaluated, seven
were more abundant inshore, four were more abundant offshore, and 24 exhibited no
horizontal trend.
Across all transects, Gray reported that more taxa and individuals were caught at
depth relative to the surface. Twenty families were more numerous at depth, four were
most abundant at the surface, and 11 showed no clear distributional pattern by depth.
Leis (1991b), in an analysis of the vertical distribution of fish larvae in the Great Barrier
Reef Lagoon, found taxon-specific patterns of vertical distribution for 50 fish taxa which
were similar overall to those reported by Gray. Most taxa had highest concentrations in
the lower portions of the water column (13-20 m) with far fewer being more abundant
near the surface (0-6 m) or at mid-depths (6-13 m). Leis reported that the vertical
distribution of fish larvae, which was highly structured during the day, was with few
exceptions nearly unstructured at night.
Gray (1993) found ontogenetic differences in the distributions of some larvae.
For example, the mean size of a larval goatfish (Liza argentea, Mugilidae) was greater
offshore than inshore and greater at the surface than at depth. Conversely, a larval jack
(Pseudocaranx dentex, Carangidae) was more abundant at depth than at the surface.
Leis (1991b) reported vertical distributions which changed little ontogenetically.
Investigations of fish larvae off coastal areas in both tropical and temperate seas
have produced results similar to Gray's in which taxa displayed different horizontal and
vertical patterns of distribution and density (Richardson et al. 1980; Leis 1982, 1986;
Kingsford and Choat 1989, Suthers and Frank 1991). For a review of larval ecology,
distributional patterns, and recruitment processes, consult Leis (1991a), Victor (1991),
Doherty (1991), and Jones (1991).
After a period of pelagic development, larvae recruit to the reef environment.
Overall, size at settlement ranges broadly, although within a family, settlement sizes of
various species can be very similar (Victor 1991). On the smaller end, Victor (1991)
recorded a mean standard length (SL) of about 4 mm for settling reef cubbyu drum
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Pareques acuminatus, while Lachner and Karnella (1980) reported sizes at settlement
of about 8 mm SL for the goby Eviota epiphanes. On the large extreme, Victor (1991)
reports collecting mature pearlfish larvae (Carapus sp.) as large as 174 mm SL, and
Leis (1978) recorded settlement lengths of almost 200 mm SL for the porcupinefish
Diodon hystrix. Victor (1991) concludes that the majority of reef species settle between
7 and 12 mm SL.
Settlement size as a percentage of size at sexual maturity and maximum size is
also quite variable. In the goby Eviota epiphanes, settlement size represents about
80% of size at sexual maturity or 50% of maximum size, which is at the upper end of
settlement size for reef fishes (Leis 1991a). Conversely, at the lower end, Bellwood and
Choat (1989) report settlement size in parrotfishes to be between 8-20% of size at
sexual maturity and 2-10% of maximum size.
How reef fishes move from the pelagic environment to the reef when they are
ready to settle is still not well understood. Unless they recruit to the reef, they will be
unable to complete their life cycle. Until relatively recently, the most widely held view
was that recruitment of fishes to the reef is a passive process in which new recruits are
dependent solely upon currents to deposit them onto the reef (Sale 1970). However,
most reef fishes are capable swimmers by the end of their pelagic phase, and it is likely
that behavior (i.e. swimming) plays a role in their finding suitable habitat (i.e. a reef) in
which to settle (Leis 1982, 1991a). Nonetheless, it is unlikely that swimming in and of
itself, can account for the movement of fishes over the vast distances (sometimes
hundreds of kilometers) necessary to find a suitable reef.
A number of physical mechanisms, summarized by Leis (1991a), have been
proposed which could assist fish larvae in returning to coral reef environments. Those
processes include: 1) mesoscale current eddies caused by flow around reefs or islands
which might return larvae to the reef [this process has been proposed by Lobel and
Robinson (1985, 1986) as being an important mechanism by which larvae from the
leeward coast of the Big Island are returned to coastal reefs]; 2) tides which may induce
eddies near points or banks, or tidal jets through narrow reef passes, both of which
could result in reefward transport of larval fishes; 3) internal waves along density
discontinuities (a thermocline) which could transport planktonic organisms shoreward;
4) localized upwelling on the leeward side of reefs which might transport deeper-living
larvae to the surface close to shore; 5) wind-driven surface layers on the windward
sides of reefs might provide a mechanism by which shallow-living larvae could return to
the reef; 6) Ekman transport within the top 100 meters could carry larvae toward shore
depending upon the position of the reef and the prevailing winds; 7) density-driven
shoreward flow of larvae living near the surface and the bottom might occur when water
column stratification breaks down nearshore due to wave turbulence but persists
offshore; and 8) Stokes transport (small net water movement in the direction of wave
propagation when water depth is less than swell wavelength) which could transport
12
surface-living larvae toward the reef.
Why is a pelagic larval stage so ubiquitous in the life-cycles of coral reef fishes
(among marine fishes in general)? Unfortunately, there is no simple clear-cut answer to
this question. A pelagic stage is almost certainly the only effective dispersal mechanism
available to most coral reef fishes. Sale (1980a) reports that juvenile and adult reef
fishes are strongly site attached and sedentary, and are hence relatively ineffectual in
regard to dispersal. Conversely, the pelagic larval phase may permit coral reef fishes to
disperse on a scale from meters to perhaps thousands of kilometers (Leis 1991a).
While dispersal may be the proximal reason for the widespread occurrence of
pelagic larvae, the ultimate reason why dispersal is advantageous remains uncertain.
In a system structured by competition for limited resources, dispersal of juveniles away
from competitively dominant adults might confer selective advantage to new recruits,
assuming that juveniles can locate vacant habitat which is suitable for survival.
However, a great deal of evidence suggests that the community structure of coral reef
fishes is rarely determined by competition for limiting resources (Ebeling and Hixon
1991; Talbot et al 1978; Hixon 1991, 1993; Sale 1977, 1980a, 1980b, 1991c; Victor
1983, 1991; Doherty and Williams 1988; Doherty 1991) which undermines the concept
of dispersal as a competition reducing adaptation (factors determining the community
structure of coral reef fishes will be explored in more detail later in this chapter).
It has been hypothesized that coral reefs are patchy, unpredictable environments
(Barlow 1981; Sale 1977, 1980a, 1980b, 1991c), and that pelagic dispersal of reef
fishes is adaptive in regard to locating patches of available habitat (Barlow 1981). In
essence, the reproductive output of adult fish is spread widely via pelagic dispersal.
Most offspring will not happen upon suitable habitat and will perish, but some will recruit
successfully. This idea of "risk spreading" has merits but there are problems with it and
its validity remains to be determined (Leis 1991a).
A number of alternate hypotheses have been postulated to account for the
prevalence of pelagic larvae in reef fishes. Pelagic dispersal away from reefs may be
an evolutionary response to intense predation pressure on coral reefs (Johannes 1978);
predation pressure which exceeds even that of the planktonic environment (see below).
It has also been proposed that the pelagic stage is an energy saving mechanism
because drifting in slow ocean currents should require less energy than swimming to
maintain position over the reef where currents are strong (Bourret et al 1979 as cited by
Leis 1991a). It has even been suggested that the pelagic stage keeps larval fishes
away from the surf zone where they could be pulverized by waves (Bakun 1986).
Whatever advantage is conferred by the pelagic larval phase, it must outweigh
the losses suffered by larvae from planktonic predation and expatriation (i.e. loss to the
open ocean or unsuitable coastal habitat). Mortality during the planktonic stage may
13
approach 100%, much of it attributable to predation by other constituents of the
plankton and adult fishes (Hunter 1984, Leis 1991a). Coupled with this high planktonic
mortality is the tendency of marine bony fishes to produce great quantities of
eggs/larvae. Sale (1980a) in reviewing data on fecundity of coral reef fishes, reports
estimates of annual egg production ranging from about 8000 (a damselfish) to over
1,000,000 (a rabbitfish). In spite of high fecundities, adult population sizes may be
determined more by what happens in the plankton than by post-recruitment processes
like competition or predation on adults and juveniles. However, this is by no means
certain and the factors which structure coral reef fish communities remain controversial.
Again, this will be discussed further later in this chapter.
Trophic Ecology of Coral Reef Fishes
Understanding the trophic ecology of coral reef fishes is important for many
reasons. Most obviously, fishes must eat to survive, and ascertaining what they eat is
therefor relevant to understanding their overall biology. Feeding by fishes can have
profound impact on the reef community as a whole. When dietary arrays of multispecies assemblages of reef fishes are evaluated, the data provide an insight into
energy flow through the coral reef community. Species that feed offshore but return to
the reef to defecate (or be consumed by other organisms) import energy to the reef.
Species that maintain feeding territories often exclude other fishes (or even some
invertebrate species) and hence influence the distribution of species over the reef.
Some species are mechanically destructive to the reef substratum when they feed and
hence are significant contributors to bioerosion on the reef.
Clearly, the tropic ecology of reef fishes is important and merits consideration.
What follows is divided into three sub-sections: herbivores, planktivores, and
carnivores. While some of these subdivisions may appear artificial from a purely trophic
perspective (i.e. piscine "planktivores" consume zooplankton and are hence
"carnivores"), they represent the major functional feeding groups within the fishes. A
section entitled "detritivores" was omitted due to a general lack of information on the
importance of detritivory in the trophic ecology of coral reef fishes.
Herbivores
Herbivory has not widely evolved in fishes. Given the fact that plant material is
abundant in shallow reef environments, the relatively low percentage of herbivorous
fishes to have evolved might, on the surface, seem paradoxical. However, extraction of
energy from plant material is very difficult for animals due largely to the indigestibility of
cellulose and the generally low protein content of most plants (Bowen 1979, Mattson
1980). The majority of fishes have remained carnivorous, most frequently consuming
prey by swallowing it whole (Schaeffer and Rosen 1961). The herbivorous fishes which
14
have evolved utilize innovative mechanisms for processing and assimilating plant
material (see Horn 1989).
Marine herbivorous fishes are not uniformly distributed throughout the marine
realm, with species richness declining from tropical to temperate regions (Horn 1989).
On temperate and boreal reefs, there are relatively few herbivorous fish species, they
are generally uncommon, and they consume only a small proportion of the reef's
primary production (Horn 1989). Dominant cold water herbivorous taxa are
invertebrates like echinoids, gastropods, and crustaceans (Choat 1991). On coral reefs
the situation is quite different.
Herbivorous fishes of coral reefs are among the most abundant and widespread
groups of vertebrate herbivores (Choat 1991). Herbivorous fishes on coral reefs
account for a large portion of the plant biomass which is removed and their effect on
reef algae and ecology is profound (Hay 1991). In fact, the groups of herbivorous fishes
that are found on coral reefs are pretty much unique to those ecosystems, not extending
beyond the boundaries of coral reefs (Horn 1989). Their seemingly obligate association
with coral reefs is sufficiently specific as to define biogeographic boundaries (Gaines
and Lubchenco 1982, Choat 1991).
Choat (1991) points out that herbivorous fishes have been implicated in three
fundamental processes on coral reefs. First, herbivores provide a link for the flow of
energy between primary producers and the reef's remaining consumers (i.e. carnivorous
trophic levels). Second, they influence the distribution, size, internal composition (see
Hay 1991), and even rate of production of plants on the reef. Finally, interactions
among territorial herbivorous fishes have been instrumental in the development of
demographic and behavioral models for reef fishes in general.
Although there are numerous families of coral reef fishes with herbivorous
representatives, most appear to be from just four fairly speciose families: Acanthuridae
- approximately 76 species, Siganidae - about 25 species, Scaridae - about 79 species,
and Pomacentridae - approximately 159 omnivorous or herbivorous species (Choat
1991). Another potentially significant group of herbivores are the blennies (Blenniidae),
although they need more study before their importance can be ascertained (Choat
1991).
There is a significant longitudinal trend in the distribution of herbivorous fishes
from the four families listed above. According to Choat (1991) most species occur in
the Indo-West Pacific region (258 species) where they are the dominant herbivorous
group. Species richness drops off markedly on the Pacific Plate (99-105 species), the
Eastern Pacific (25 species), the Caribbean (29 species), and the East Atlantic (10
species). On coral reefs outside the Indo-west Pacific, the relative ecological impact of
herbivorous fishes may be shared with other groups (Sale 1980a). For example, in the
15
Caribbean, echinoids and fishes are both important herbivorous taxa (Carpenter 1986).
Herbivorous fishes have characteristic structural features related to their trophic
life-style (Choat 1991). Like many percoid fishes, they are deep-bodied with marked
lateral compression, a body form thought in part to facilitate maneuverability in the
complex relief of a reef environment. The bones and associated muscles supporting
the pectoral fins are well developed, and the pelvic fins are thoracic (i.e. located
immediately below the pectoral fins). The pectoral fins are frequently used for
locomotion and orientation during feeding (Choat 1991). The thoracic placement of the
pelvic fins facilitates hydrodynamic stability during deceleration caused by extension of
pectoral fins (Marshall, 1965).
In general, the mouths of herbivorous fishes are small and terminal in location.
During feeding, pronounced expansion of the oral cavity does not occur, in contrast to
carnivorous fishes which frequently expand the oral cavity as they open their mouths to
suck in prey (Choat 1991). The teeth of herbivorous fishes tend to be small and incisorlike, are frequently fused in some fashion, and may even form beak-like structures as in
the parrotfishes (Choat 1991).
Herbivores have been grouped, according to their potential impact on the algae
they consume, into three functional groups: 1) scraping herbivores, 2) denuding
herbivores, and 3) non-denuding herbivores (Steneck 1988). Scraping herbivores, like
parrotfishes and certain urchins (Diadema), have the greatest impact on algal
abundance and also feed on the widest array of algal species. Denuding herbivores,
like rabbitfishes and surgeonfishes, can significantly reduce algal biomass when they
occur in high densities. Fishes of this group cannot feed on crustose coralline algae
and have limited abilities to forage on articulated corallines or leathery macroalgae
(Steneck 1988). Non-denuding herbivores, like most damselfishes, exhibit limited ability
to significantly reduce algal biomass.
Processing of ingested algae (i.e. crushing of cell walls) is not done by the teeth.
Instead other internal structures are used like the well-developed pharyngeal plates of
labroids (Scaridae and Pomacentridae) or gizzard-like structures in the alimentary canal
of acanthuroids (Acanthuridae and Siganidae). Energy is probably extracted from algae
by a number of mechanisms including mechanical trituration, acid digestion, and
probably microbial fermentation (Lobel 1981, Rimmer and Wiebe 1987, Choat 1991).
Unfortunately, there is limited information available on the importance of
endosymbionts in digestion of plant material by fishes (Choat 1991). Among suggested
criteria for utilization of endosymbionts are constant food supply and a slow transit time
through the gut to facilitate microbial reproduction (Horn 1989). Not all coral reef
herbivores meet these criteria. Surgeonfishes, for example, have gut transit times of
only two to four hours (Choat 1991). Yet there is evidence that surgeonfish alimentary
16
tracts harbor both protistan and bacterial endosymbionts which probably facilitate the
digestion of ingested plant material (Fishelson et al 1985, Clements et al 1989, Sutton
and Clements 1988, Choat 1991). At present, more work needs to be done before
digestion and assimilation of plant matter by coral reef herbivores is adequately
understood (Horn 1989, Choat 1991).
Herbivorous fish foraging is generally marked by continuous rapid grazing over
small areas of reef substratum. The most likely targets of this grazing activity are algal
turfs and mats, and accumulated organic material (Russ and St. John 1988). The most
abundant algal material on reefs are multi-species turfs less that 10 mm in height
composed primarily of diminutive filamentous species (Scott and Russ 1987, Steneck
1988, Choat 1991). These turfs also harbor benthonic diatoms, bacteria, and organic
detritus. Crustose algae are also present, usually growing on exposed substratum
(Littler and Littler 1984; Steneck 1982, 1988; Choat 1991). Algal thalli greater than 10
mm in height ("macroalgae") are relatively rare on reefs (Lewis 1986, Choat 1991).
Other potential sources of energy for herbivorous coral reef fishes include algal mats
growing on sand and rubble, sea grasses, symbiotic algae associated with sessile
invertebrates, and perhaps organic detritus (Choat 1991).
Herbivore grazing is most intense on coral reefs in shallow areas between about
1-5 meters of depth, with grazing intensity exhibiting a relatively linear decline with
increasing depth (Steneck 1988). In areas of intense grazing, algal biomass is low and
dominated by turfs and crustose coralline algae (Scott and Russ 1987, Steneck 1988,
Choat 1991). Despite the low algal biomass present on most coral reefs, the extremely
high growth rates of many algae species make shallow coral reefs among the most
productive habitats on earth, with much of this productivity being consumed by
herbivorous fishes (Hay 1991). On intensely grazed areas (i.e. shallow fore reefs)
fishes may take up to 156,000 feeding bites/m2/day and consume from 50-100% of the
total algal production (Hay 1991).
Algal biomass is often greatest at or just above MLW where herbivory is low and
exhibits a secondary biomass peak at depths greater than 30 m (Earle 1972, Steneck
1988). In areas experiencing reduced herbivory due to strong wave action,
experimental exclusion of herbivores, or heavy fishing of herbivores, algal biomass
increases and more macroalgae are present (Steneck 1988). In essence, with
increased grazing from scraping and denuding herbivores, algal biomass decreases,
and algal groups shift from macroalgae, to turfs, and finally to crustose coralline algae
(Steneck 1988).
Reef algae have evolved a number defensive "strategies" which enable them to
coexist with herbivores. Steneck (1988) describes three basic defensive strategies
which are exhibited by algae. The first is resistance to consumption by being
structurally difficult to eat. This is the fundamental strategy of the coralline algae. The
17
second is recovery after being partially consumed and is characteristic of algae capable
of rapid growth and regeneration. This is a primary strategy for multi-species turfs. The
third strategy is deterrence against being consumed by being unpalatable. Many algae,
especially fleshy macroalgae, retain noxious or toxic chemical compounds (secondary
metabolites) in their tissues so that herbivores learn to avoid them. These three
strategies are not mutually exclusive and many algae species may use more than one
to deter herbivores (Steneck 1988, Hay 1991).
A significant physical effect of herbivory by reef fishes is bioerosion which is the
degradation of the reef matrix by biological processes (Choat 1991). Both parrotfishes
and surgeonfishes have been identified as major bioeroders and sediment producers on
coral reefs (Horn 1989, Hutchings 1986). During the grazing process, reef matrix or
living coral is scraped up or excavated by foraging fish. These materials are reduced to
sediment which is passed through the alimentary tract and redistributed over the reef
surface via defecation (Choat 1991). Bioerosion from grazing herbivorous fishes may
be an important agent of structural change on coral reefs (Choat 1991).
For a more thorough treatment of herbivory by marine fishes and its effects on
algae and reef structure refer to reviews by Steneck (1988), Horn (1989), Choat (1991),
and Hay (1991).
Planktivores
The majority of marine fishes consume plankton during their juvenile phase,
although most of these shift to other types of food as they mature (Leis 1991a).
However, on coral reefs adult fishes adapted for feeding on zooplankton are quite
common and are of major importance to the trophic economy of the coral reef
community (Hobson 1991). Coral reefs have adult planktivorous fishes which are active
during both day and night, although each period has its own array of species. Virtually
every major acanthopterygian (spiny rayed fishes) family present on coral reefs includes
species specialized as planktivores (Hobson 1991). However, some families have
many species adapted for planktivory. For example, there are many diurnal
planktivores among the sea basses (Serranidae), the butterflyfishes (Chaetodontidae),
the damselfishes (Pomacentridae), and the trigger/file fishes (Balistidae), while there
are many nocturnal planktivores among the squirrel/soldierfishes (Holocentridae), the
big-eyes (Priacanthidae), and the cardinalfishes (Apogonidae) (Starck and Davis 1966;
Randall 1967; Hobson 1974, 1991). Day-active and night-active planktivores are
generally quite dissimilar, not only taxonomically, but both structurally and behaviorally
(Hobson 1991). Diurnal and nocturnal planktivores are compared below, beginning with
diurnal planktivores.
Diurnal planktivores have diverged much from the generalized, large-mouthed
carnivorous ancestors hypothesized for teleost fishes by Schaeffer and Rosen (1961)
18
and Gosline (1971). In general, diurnal planktivores possess small, upturned mouths,
with highly protrusile, though toothless jaws (Davis and Birdsong 1973, Hobson 1991).
The oblique positioning of the mouth, which shortens the snout, appears to place both
eyes in a position to focus simultaneously on prey giving them the depth perception of
binocular vision (Hobson 1991). Coupled with mouth adaptations, are closely spaced,
long gill rakers which prevent small ingested prey from escaping through the gill
openings. In essence, diurnal planktivores are adapted to target individual zooplankters
which are then either sucked in or engulfed by the jaws (Hobson 1991).
The diet of diurnal planktivorous fishes consists primarily of small swimming
crustaceans, especially calanoid and cyclopoid copepods (Hobson and Chess 1978,
Hobson 1991). Zooplankters taken by reef fishes during the day tend to be transparent
due to reduced pigment concentrations and are virtually all less than 3 mm in their
greatest dimension, with many being <1 mm maximum dimension (Hobson 1991). A
large proportion of the zooplankton that are consumed by diurnal planktivores are
"transient" individuals from the open ocean which are carried to the reef by currents
(Hobson 1991).
Because diurnal planktivores consume large quantities of open ocean plankton, it
has long been postulated that planktivorous fishes are a major trophic link between the
coral reef and the open sea (Emery 1968, Davis and Birdsong 1973). There are at least
three ways in which energy captured by planktivorous fishes might find its way to other
elements of the coral reef community. First, some planktivores may be consumed by
larger piscivorous fishes (Choat 1968, Hartline et al. 1972, Polovina 1984). A second,
and probably the major path of energy flow from diurnal planktivores to other reef
organisms is through their feces (Hobson 1991). Feeding planktivores produce large
amounts of feces (sometimes containing largely undigested zooplankton) which "rain
down" upon the reef and are consumed by other fishes as well as benthonic herbivores
and detritivores (Hobson 1991, Robertson 1982). Also, a temperate zone diurnal
planktivorous pomacentrid (Chromis punctipinnis) has been reported to defecate in
nocturnal shelters on the reef in southern California, with fecal matter accounting for the
importation of about 8 grams of carbon per square meter per year in that environment
(Bray et al. 1981). Bray and his colleagues hypothesize that this form of energy
importation to the benthos is likely to be even more significant on tropical coral reefs
where diurnal planktivores are common and shelter on the reef at night. A third way in
which diurnal planktivores may transfer energy to the reef is through death (attributable
to sickness or senescence) and subsequent decay.
Although the mouth structure of diurnal planktivores exhibits a high degree of
convergence, body shape can be quite different among the various species, and
frequently correlates to where a particular species forages on the reef. Most diurnal
planktivores maintain station over a section of reef and simply consume individual
zooplankters as they drift by with the current. Many unrelated diurnal planktivores
19
possess streamlined bodies and forked caudal fins which are adaptations which
enhance swimming speed (Norman and Greenwood 1963). The degree of streamlining
and forking increases in species that forage successively farther from the reef (Hobson
1991). The streamlining helps these species maintain station in the stronger currents
which flow along the outer edge of the reef and also enables them to rapidly flee to the
safety of the reef at the approach of a potential predator (Hobson 1991).
Not all diurnal planktivores exhibit bodies which are more streamlined than their
benthic relatives. Some pomacentrid planktivores (Dascyllus spp. and
Amblyglyphidodon spp.) are deeper-bodied and have longer spines than their benthonic
relatives (Hobson and Chess 1978). In addition, planktivorous chaetodontids and
pomacanthids (angelfishes) are as deep bodied as their benthonic counterparts
(Hobson and Chave 1990). Although this body form is probably not as suitable as a
streamlined body in regard to maintaining station in strong currents, it is likely to be an
effective deterrent to predators because of the tendency of deep-bodied fishes to lodge
in the mouth or pharynx of fishes that attempt to swallow them (Hobson 1991).
Planktivorous fishes also exhibit a tendency to be distributed on the basis of size,
with larger individuals characteristically feeding close to the reef edge (Hobson 1991).
Hobson (1974) in his study of feeding by fishes on the coral reefs off Kona, Hawaii
found that the larger species (>10 cm SL) of planktivores were more common near the
drop-off at a depth of about 25 meters. Citing that work, Hobson (1991) lists those
species as Chaetodon miliaris, Hemitaurichthys polylepis, Chromis verater, Acanthurus
thompsoni, Naso hexacanthus, and Xanthichthys auromarginatus. These species were
scarce in the waters above the shallower inner reef, while smaller planktivores like
Chromis agilis and C. hanui (approximately 7 cm SL maximum size), though numerous
at the drop-off, were also abundant in shallower water. In summary, at the reef drop-off
there were 12 species of diurnal planktivore constituting 45% of the fishes counted,
while over the inner reef there were only 6 planktivrous species comprising just 14.6%
of the fishes counted (Hobson 1991).
Hobson and Chess (1978, 1986) reported similar size-related distributions for
diurnal planktivores in the waters off Enewetak atoll. At Enewetak, plankton prey size
correlated to feeding location, with fishes feeding in deeper water (larger fishes) taking
larger zooplankters (2.5-3.0 mm maximum dimension), and fishes feeding in shallower
waters (smaller fishes) taking smaller arrays of zooplankton (about 1.0 mm maximum
dimension).
Diurnal planktivorous fishes commonly form aggregations when they are feeding
in open water (Hobson 1991). It has long been recognized that aggregation may afford
fishes some defense against predators (Hobson 1968, Hamilton 1971, Shaw 1978).
Hobson (1991) reports that if approached by a large piscivore (i.e. Caranx spp.),
aggregations of diurnal planktivores rapidly condense and often swim rapidly toward the
20
bottom.
In addition to forming aggregations as an anti-predatory adaptation, diurnal
planktivores modify their position in the water-column in response to light. Fishes in the
water-column become increasingly susceptible to successful attack by larger
piscivorous fishes as ambient light intensity drops (Hobson 1972). Diurnal planktivores
respond by foraging closer to the bottom when the sky is overcast compared to bright
sunlight, and on clear days will briefly descend toward the bottom when clouds pass in
front of the sun (Hobson 1991). In fact, at dawn and dusk there is a complete
changeover between the diurnal and nocturnal fish faunas on coral reefs which is lightintensity mediated, highly structured, and ultimately in response to the threat of
predation by piscivorous fishes (Hobson 1972). This will be discussed further at the end
of the next subsection.
Nocturnal planktivorous fishes have experienced markedly different selection
pressures compared to their diurnal counterparts and as a result are really quite
different in body morphology, diet, and their distribution over the reef. The fundamental
problem facing nocturnal planktivores is visual location of small prey in the dim light of
night (Hobson 1991). Almost universally, they have exceptionally large and sensitive
eyes as is evidenced by the soldierfishes, the big-eyes, and the cardinalfishes.
However, in increasing visual sensitivity, nocturnal fishes have sacrificed some acuity
(the ability to resolve images) and, relative to diurnal planktivores, are probably limited
in their ability to resolve smaller objects (Munz and McFarland 1973, McFarland 1991,
Hobson 1991). In conjunction with the inability to resolve smaller objects, nocturnal
planktivores have not evolved the small mouths and binocular vision used by diurnal
planktivores to select and engulf individual small zooplankters. Instead, their mouths
are relatively large and terminal, having diverged little from the generalized, largemouthed carnivorous ancestors hypothesized for teleost fishes by Schaeffer and Rosen
(1961) and Gosline (1971).
The diet of nocturnal planktivorous fishes consists primarily of relatively large
zooplankton (>2 mm maximum dimension), which are taken not so much as a result of
preference for larger prey, but rather because of the inability of these fishes to see and
therefor consume smaller zooplankton species (Hobson 1991). As a result of visual
limitations, small open-ocean zooplankton which comprise the major prey of diurnal
planktivores and which are actually more abundant at night compared to day, are
essentially absent from the diets of nocturnal planktivores (Hobson and Chess 1978,
1986; Hobson 1991). Planktonic prey that are taken by nocturnal planktivores include
semipelagic residents of the reef which rise into the water column during the night,
larger holoplanktonic residents like mysids, and some large open-ocean plankton like
euphausids (Hobson 1974, Hobson and Chess 1978, Gladfelter 1979). Many of the
resident zooplankton, in addition to larger size, are opaque or awkward swimmers which
makes them appropriate targets in the dim nocturnal light (Hobson 1991).
21
Nocturnal planktivores that consume resident zooplankton are not, like their
diurnal counterparts, a major trophic link between the open ocean and coral reef
community. However, not all nocturnal planktivorous fishes feed exclusively over the
coral reef, and within a particular species, some individuals may leave the reef to feed
offshore. For example, Hobson (1991) reports that some Priacanthus cruentatus,
Myripristis murdjan, and M. amaenus from Hawaiian reefs migrate seaward at night to
feed on larger open-ocean zooplankton and other pelagic organisms like cephalopods.
Those individuals, of course, do represent a direct trophic link between the open-ocean
and the coral reef. Hobson (1991) maintains that, unlike diurnal planktivores, the feces
of nocturnal planktivores are probably not the primary way that energy is passed on to
other segments of the reef. Feces are hard to see at night, which probably limits
coprophagy by other fishes. Also, nocturnal planktivores take larger and fewer prey,
digestion is slower, and defecation less frequent. Finally, nocturnal planktivores do not
aggregate like their diurnal counterparts which greatly facilitates coprophagy during the
day. The flow of energy from nocturnal planktivores to other elements of the coral reef
community may go primarily through piscivorous predators (Hobson 1991).
Nocturnal planktivores are more widely dispersed over the reef than diurnal
planktivores. At dusk, they leave shelter sites (holes, crevices, caves, etc) to feed
nearby or migrate to feeding areas elsewhere (Hobson 1972). They do not appear to
form aggregations which are so characteristic of diurnal species, instead dispersing to
forage individually or in small, loosely associated groups (Hobson 1991). Their
nocturnal prey, rather than being most available in the currents at the edge of the reef,
are widespread over the reef, so aggregation in response to a clumped food resource
doesn't occur. The threat from visual predators is apparently much reduced at night, so
aggregation as a defensive response to predators also doesn't occur (Hobson 1991).
Morphologically, nocturnal planktivores lack the streamlined bodies and forked tails
characteristics of fast swimming fishes, which suggests that maintaining station in a
strong current (or rapid swimming to escape a predator) is not a problem regularly
encountered by these fishes.
For a thorough review of planktivory by fishes inhabiting coral reef ecosystems,
see Hobson (1991).
Carnivores
Carnivorous fishes exhibit an amazing array feeding morphologies, from the tiny,
specialized mouths of fishes like forceps butterflyfishes (Forcipiger spp.) to the large,
generalized mouth structure common in so many species of scorpionfish
(Scorpaenidae), snapper (Lutjanidae) and sea bass (Serranidae). As might be
expected from the diverse feeding morphologies, the range of prey items taken includes
both invertebrates (sessile and mobile, from hard and soft bottom habitats) as well as
22
fishes. Vertebrates other than fishes may also be taken by some species. Juvenile
turtles may be consumed by reef fishes shortly after hatching, while adult turtles are
taken by large sharks, especially the tiger shark (Galeocerdo cuvier). In addition, birds
(especially newly fledged individuals) may be taken by sharks like the tiger shark.
Carnivorous species of reef fishes are more common on coral reefs than their
herbivorous or planktivorous counterparts. Jones et al. (1991), in their review of fish
predation and its impact, evaluated data from seven studies on the diets of coral reef
fishes (Hiatt and Strasburg 1960, Randall 1967, Goldman and Talbot 1976, Hobson
1974, Williams and Hatcher 1983, Sano et al. 1984, and Thresher and Colin 1986), and
calculated the proportion of fish species in different trophic categories. Carnivorous
species (piscivores and benthic invertebrate feeders, not including planktivorous
species) were the most common in all seven investigations, ranging from a high of 68%
of the species present to a low of 41%. Herbivores ranged from about 25% to 7% of
species present, planktivores ranged from 38% to 4%, and omnivores ranged from 19%
to 4%.
Among carnivores, fishes specialized to consume benthic reef invertebrates
appear to be more prevalent than piscivores. In five of the seven feeding studies cited
by Jones et al (1991), benthic invertebrate predators were the most speciose trophic
group, accounting for between 56% and 27% of the species present. Piscivores
comprised between 37% and 4% of the species present in those studies. Invertebrate
predators and piscivores are discussed below, beginning with fishes that feed on
invertebrates.
Major categories of fishes that feed on benthonic invertebrates include coralpolyp feeders, sessile invertebrate feeders, feeders on mobile invertebrates, and
omnivores which are frequently primarily carnivorous (Jones et al. 1991). Fishes which
feed on mobile invertebrates are far more numerous than those consuming coral polyps
or other sessile invertebrates [45-34% of the species in the seven studies cited by
Jones et al. (1991) versus 9%-1% and 13%-3% for the other two categories
respectively].
Among mobile invertebrates, crustaceans may be particularly important prey on
coral reefs. For example, in their study of fishes from the Northwestern Hawaiian
Islands, Parrish et al. (1985) found that benthic crustaceans comprised 75% of the
dietary items consumed by percent occurrence in stomachs (53% by numbers, 48% by
weight), and consisted mainly of crabs (about half), followed by shrimps, amphipods,
and stomatopods. Molluscs were a distant second to crustaceans as dietary items
(21.5% by occurrence, 21.3% by numbers, and 11.1% by weight), with other benthonic
invertebrate taxa like polychaetes and echinoderms rarely showing up in stomach
contents (<5% by any measure). Fishes foraging over soft sediments for mobile
invertebrate prey appear to consume mainly molluscs (G. P. Jones, D. J. Ferrell, and P.
23
F. Sale, unpublished observations as cited by Jones et al. 1991).
Benthonic invertebrate predators may exhibit selectivity in prey items consumed
(i.e. the relative abundance of prey items in their diets does not simply mirror prey
abundances in the environment), although relatively few investigators have
quantitatively estimated prey abundances for comparison with dietary arrays (Jones et
al. 1991). Parrish et al. (1985) sampled the benthic biota of patch reef habitats in the
Northwestern Hawaiian Islands for comparison with their fish dietary data. Their results
suggest that crustaceans and molluscs are targeted by invertebrate feeding fishes
(Jones et al. 1991). Crustaceans were almost twice as abundant by weight in fish
stomachs compared to their field abundance, while molluscs were almost four times
more abundant by weight in fish stomachs than in the field. Conversely, echinoderms,
worms, and sponges were much more abundant in the field than in the stomachs of
fishes, suggesting avoidance of these taxa. Guzman and Robertson (1989) compared
coral availability to coral consumption by the corallivorous pufferfish Arothron meleagris
in the eastern Pacific. Their results indicated that coral consumption by this fish was not
simply a reflection of coral species abundance. Feeding preference for various coral
species varied between study locations. At some locations, common corals (Pocillopora
and Porites) made up the bulk of the diet while at others, rare corals (Psammocora)
made up the bulk of the diet. Furthermore, the relative proportion of corals consumed
was subject to change with time and not related in a consistent way to changes in
abundance.
Foraging by sessile invertebrate feeding fishes can have a pronounced impact on
the distribution and abundance of their prey (Jones et al. 1991). Sponge distributions
may be influenced by the action of grazing carnivores, with sponge populations being
confined to areas where grazing pressure is less intense (Bakus 1964 as cited by Jones
et al. 1991). Grazing carnivores can also effect overall species diversity in sessile
invertebrate communities (Jones et al. 1991). In a series of experimental manipulations
inside caves at Heron Island, Day (1977, 1985) was able to demonstrate that areas
grazed by fishes had invertebrate species diversity approximately 20% higher than in
experimental plots where grazing was prevented by cages. Fishes (primarily
pomacanthids and balistids), in preferentially selecting ascidians (tunicates), increased
survival of competitively inferior encrusting fauna like bryozoans.
Coral feeding fishes can effect corals in a direct negative way (i.e. by consuming
them), or in indirect ways either positive or negative (i.e. by altering the outcome of
competition between coral species through their foraging activities) (Glynn 1988, 1990).
Corallivorous fishes can exhibit profound direct effects on the distribution of their coral
prey. For example, in Guam the coral Pocillopora damicornis suffers a pronounced
reduction in its potential depth distribution as a result of predation from corallivorous
fishes (Neudecker 1977). While able to survive in water 30 m deep, and grow rapidly at
15 m of depth, the coral is essentially restricted to the reef flat, crest, and lagoons
24
because of intense predation pressure by corallivorous fishes in deeper water.
Selective predation by fishes on competitively dominant corals (direct effect) can
provide a competitive release for subordinate coral species (indirect effect) (Glynn 1988,
1990, Lang and Chornesky 1990). Cox (1986) investigated the effect of predation by
the corallivorous butterfly fish, Chaetodon unimaculatus, on competition between
Montipora verrucosa and Porites compressa in Kaneohe Bay, Hawaii. She found that
C. unimaculatus, which preferentially feeds on the competitively dominant M. verrucosa,
reduces competitive stress on the subordinate P. compressa. In the presence of the
corallivore, P. compressa enjoyed increased abundance and distribution.
Fishes feeding on mobile invertebrates can also influence the distribution and
abundance of prey species (Jones et al. 1991). For example, in coral reefs off of Kenya
it appears that the abundance and distribution of urchins, primarily boring urchins
(Echinometra mathaei), is markedly affected by predation from fishes (McClanahan and
Muthiga 1989, McClanahan and Shafir 1990). On four reefs historically subject to
heavy fishing, fish densities were low and urchin densities were high. On two reefs
where fishes were protected, fish densities were about 4x higher and urchin densities
about 100x lower. McClanahan and Muthiga (1989) attributed 90% of urchin mortality in
Kenya to predatory fishes. McClanahan and Shafir (1990) identified the balistids
Balistaphus undulatus and Rhinecanthus aculeatus as the dominant fish predators
involved. On natural (unfished) reefs, boring urchins were found primarily on the reef
flat with numbers declining sharply with depth (McClanahan and Muthiga 1989). The
decline was attributed to increased predation pressure by fishes in deeper regions of
the reef. On fished reefs where piscine predation on the urchins was reduced, E.
mathaei expanded its distribution into deeper water.
The effects of predation by fishes on invertebrates may not only relate to
consumption of their prey, but also to disturbance of the habitat by the foraging fishes
which may effect neighboring invertebrates (Jones et al. 1991). Unfortunately,
separating these two sources of impact is often very difficult (Jones et al. 1988).
It appears that predation by fishes may influence the distribution, abundance,
and species diversity of benthonic invertebrates on coral reefs as well as operating as a
major selective force leading to the evolution of defensive mechanisms by invertebrate
prey (Bakus 1966, 1969, 1981, 1983 as cited by Jones et al. 1991). Additionally, it has
been hypothesized that the influence of fish predation on invertebrate communities
increases from temperate to tropical systems (Bakus and Green 1974; Green 1977;
Vermeij and Veil 1978; Bakus 1964, 1981, 1983; Bertness 1981 as cited by Jones et al.
1991). Unfortunately, much of the work done to date in the area of fish predation on
invertebrates is from temperate systems or focuses on trophic groups other than those
consuming benthonic invertebrates (Jones et al. 1991). More work needs to be done
before the impact of piscine predators on coral reef invertebrates is fully understood
25
(Jones et al. 1991).
Piscivorous fishes, although not as prevalent as invertebrate feeders, are still
relatively common on coral reefs. Hixon (1991), citing data from nine regional surveys
of coral reef fish diets (Hiatt and Strasburg 1960, Talbot 1965, Randall 1967, Hobson
1974, Goldman and Talbot 1976, Brock et al. 1979, Harmelin-Vivien 1981, Williams and
Hatcher 1983, and Parrish et al. 1986) reports that 8% to 53% of the fish species on
coral reefs consume other fishes, at least as part of their normal diet. Hixon (1991)
goes on to point out that piscivorous fishes are sometimes very abundant in addition to
being diverse, citing work by Goldman and Talbot (1976) which reported that piscivores
accounted for 54% of the total fish biomass at One Tree Island on the Great Barrier
Reef. Clearly, fishes which consume other fishes, are an important trophic group on
coral reefs.
Morphologically, piscivores have for the most part remained fairly close to the
generalized, large-mouthed carnivorous ancestors hypothesized for teleost fishes by
Schaeffer and Rosen (1961) and Gosline (1971), although some groups exhibit
structural specializations related to feeding like tubular mouths (i.e. trumpetfishes) or
highly modified body morphology (i.e. frogfishes). Most piscivores have large mouths,
with jaws exhibiting various degrees of protrusibility. Many, though not all, have
distendable buccal cavities, which enlarge when they strike creating a sucking action
which may facilitate the capture of prey. Most possess conical, inward-slanting teeth for
piercing and holding piscine prey prior to swallowing them whole (Lagler et al. 1977).
The gill-rakers of piscivores (and many other carnivores) are short, stout, and widely
spaced (Moyle and Cech 1988). The pharynx of piscivores is usually large and
distendable, and their stomachs tend to be elongate and tubular in shape (Lagler et al.
1977). The gut is short indicative of the digestibility of piscine prey (Lagler et al. 1977,
Moyle and Cech 1988).
Behaviorally, piscivores exhibit diverse foraging strategies. Hixon (1991)
referring to the work of Hobson (1975, 1979) outlined five major piscivore feeding
categories: 1) open-water species like jacks which pursue their prey (Potts 1981); 2)
cryptic species like lizardfishes and scorpionfishes which ambush their prey (Sweatman
1984); 3) species like groupers and snappers which seem to habituate prey to the
illusion that they are nonpredatory (Harmelin-Vivien and Bouchon 1976); 4) species like
trumpetfishes which slowly stalk their prey (Kaufman 1976); and 5) species like moray
eels that locate prey within crevices (Bardach et al. 1959). These various hunting
strategies are not necessarily mutually exclusive and the final attack by all piscivores
involves a sudden and extremely rapid strike (Hixon 1991).
Additionally, some species utilize aggressive mimicry to capture prey (Hixon
1991). Aggressive mimics lull prey into complacency by resembling nonpiscivorous
species or lure prey by resembling, in some way, prey items. Trumpetfish have been
26
reported to exhibit the former type of aggressive mimicry by hiding among herbivorous
fishes (Aronson 1983). As an example of the latter variety of aggressive mimicry, the
scorpionfish Iracundus signifer lures other piscivores to their deaths by slowly moving
their dorsal fin which resembles a small fish (Shallenberger and Madden 1973).
Perhaps the most amazing of the piscivorous aggressive mimics are the frogfishes
which capture prey fishes by waving a lure-like dorsal fin spine in front of their mouths
(Pietsch and Grobecker 1978).
Prey fishes have evolved numerous anti-predatory adaptations. Hixon (1991), in
his review of fish predation and its impact on the community structure of coral reef
fishes, summarized the adaptive responses of prey fishes to predation pressure from
reef piscivores. The basic categories of defensive response outlined and discussed by
Hixon were morphological, chemical, and behavioral.
Morphological adaptations include both structural features and coloration. As
previously mentioned, many reef fishes are very deep bodied (damselfishes,
angelfishes, butterflyfishes, trigger/filefishes, etc.). Combined with spinous fin rays,
these fishes are presumedly difficult to swallow, especially if taken from behind which
causes the rear-ward projecting spines to catch in the throat and further erect. Some
fishes are able to dramatically increase body size by inflation (puffers, porcupinefishes),
thereby making it very difficult for predators to swallow them. Finally, some prey fishes
utilize a streamlined body and rapid swimming to elude fast swimming piscivores
(Hobson and Chess 1978). Young parrotfishes may deter nocturnal predation by moray
eels by secreting a mucus "cocoon" which presumedly prevents the olfactory-oriented
morays from detecting their scent while they lay inactive on the bottom (Winn and
Bardach 1959).
Coloration can be used in a variety of ways to deter predators. Cryptic coloration
(camouflage) is widespread among benthic reef fishes (gobies, blennies,
scorpionfishes, flatfishes, etc.) allowing them to match the background or to resemble
inedible objects like stones or sea grasses (Randall and Randall 1960, Hixon 1991).
Many reef fishes have alternating bright and dark colored bars on their bodies (i.e.
juvenile angelfishes, scorpidids, some damselfishes) which are thought to camouflage
the individual by disrupting its outline when viewed against features of the bottom or
other similarly colored individuals (Lagler et al. 1977). False eye spots on the tail
combined with coloration masking the eye (i.e. some butterflyfishes and anglefishes)
may cause predators to misdirect attacks (Lagler et al. 1977, Neudecker 1989). Some
prey species utilize Batesian mimicry (i.e. a harmless or palatable species mimicking a
harmful or unpalatable species) to avoid predators. For example, the plesiopid
Calloplesiops altevelis, when startled exhibits behavior and coloration which mimics the
spotted moray eel, Gymnothorax meleagris (McCosker 1977). In another example of
Batesian mimicry, the cardinalfish Fowleria sp. (harmless mimic) resembles the
scorpionfish Scorpaenodes guamensis (venomous model) (Seigel and Adamson 1983).
27
Finally, some fishes exhibit aposematic coloration (warning coloration) advertising the
fact that they are venomous (pectoral flashing by some scorpionfishes, directive
markings near the caudal "blades" of some surgeonfishes), toxic (some puffers), or
unpalatable (some butterflyfishes) (Neudecker 1989, Hixon 1991).
Venoms and toxins, often combined with aposematic coloration, may deter
piscivores. For example, all scorpionfishes (Scorpaenidae) possess venomous fin
spines. Most tropical species are cryptically colored, and many are ambush predators
on other fishes. However, if alarmed, many of these cryptic fishes suddenly erect their
fin spines and expose brightly colored pectoral fin axillary surfaces with rapid "flashing"
movements (personal observation). This startling display, combined with the fact that
they are venomous, probably deters predators. Venomous weeverfishes (Trachinidae)
are reported to exhibit warning displays when alarmed (Bond 1979), and the blennid
Meiacanthus atrodorsalis has a venomous bite (Losey 1972). Furthermore, many fishes
have toxic tissues or excretions which are thought to deter predators. The most
notorious of those are the Tetraodontiformes (pufferfishes and their allies) which have
the potent neurotoxin, tetrodotoxin, in their tissues (Halstead 1978, Gladstone 1987,
Hixon 1991). Other fishes reported to possess toxins in their skin include some moray
eels, soapfishes, some gobies, and some flatfishes (Hixon 1991).
Prey fishes have evolved a host of different anti-predatory behavioral adaptations
in response to piscivores. Beyond the obvious adaptations of staying near shelter and
flight at the moment of attack, fishes exhibit more subtle anti-predatory behaviors
including schooling, and temporal adjustment of spawning and daily activity patterns to
minimize the effect of predators (Hixon 1991). While schooling may afford fishes
adaptive advantages other than just anti-predatory benefits (i.e. improved foraging
success, hydro-dynamic drag reduction), there is widespread agreement that avoiding
predation is a major reason why so many reef fishes school or aggregate (Hixon 1991).
Among the anti-predatory advantages of schooling are: 1) aggregated prey have a
reduced probability of encountering random search predators compared to dispersed
prey; 2) for each individual there is a reduced mathematical probability of being
consumed when a predator does attack; 3) predator "misses" increase relative to strikes
on isolated prey presumedly because predators have a difficult time visually "locking
onto" any one individual among the moving mass of prey; and 4) most individuals in the
school begin to take evasive action before ever seeing the attacking predator because
all fishes in the school respond almost instantly to the evasive actions of individuals on
the edge of the school who have seen the approaching predator (Hamilton 1971, Shaw
1978, Partridge 1982, Pitcher 1986, Hixon 1991).
Beyond schooling, reef fishes reduce the effect of predation by adjusting
important activities in response to the threat from predators. Hixon (1991) citing the
work of Johannes (1978, 1981) points out that most reproductive behaviors exhibited by
tropical reef fishes appear to be designed to reduce predation on themselves or their
28
eggs/larvae. For broadcast spawners (most marine fishes), offshore spawning
migrations reduce predation on eggs/larvae, spawning near shelters reduces predation
on the spawners, vertical spawning rushes reduce the time spawners are exposed and
reduces predation on eggs by releasing them away from the bottom, spawning during
ebbing spring tides reduces predation on eggs/larvae because tidal action moves them
offshore, and spawning at night reduces predation on both spawners and eggs.
Demersal spawners defend their broods which reduces predation on eggs, and livebearers eliminate predation on eggs/larvae.
Finally, tropical reef fishes adjust their basic daily activity patterns to minimize the
effect of visual piscivores (Hobson 1972, Collette and Talbot 1972, Domm and Domm
1973). Basically, during the twilight periods of dawn and dusk, fishes susceptible to
predation by visual predators are inactive in shelters on the reef. These twilight periods
of inactivity, each lasting about 15 minutes, were coined the "Quiet Period" by Hobson
(1972). On the Kona Coast of Hawaii, the evening quiet period occurs approximately
15-30 minutes after sunset, while the dawn quiet period lasts from about 45-30 minutes
before sunrise (Hobson 1972). During these crepuscular periods, the visual systems of
both diurnal and nocturnal prey fishes are ineffective for detecting piscivores
(McFarland 1991). Conversely, the visual systems of piscivores achieve maximum
sensitivity at twilight (Hixon 1991). The threat of predation during crepuscular hours has
resulted in rigid structuring of the activity patterns of both diurnal and nocturnal prey
fishes, mandating relative inactivity during the period of greatest piscivore advantage
(Hobson 1972).
For a more thorough review of the effects of carnivorous fishes on coral reef
ecosystems, see Jones et al. (1991) and Hixon (1991). Diurnal activity patterns in
Hawaiian reef fishes are covered in detail by Hobson (1972) and summarized by
Hobson (1991).
Patterns of Spacing in Coral Reef Fishes
How coral reef fishes are distributed spatially in their environment is an important
aspect of their social structure and can provide clues to their natural history. Spacing
patterns in coral reef fishes are diverse, ranging between solitary species which do not
regularly interact socially with conspecifics to species which form social groupings like
aggregations of territorial individuals or aggregations/schools of nonterritorial
individuals. As important as spacing is, it is only one aspect of the social organization
or structure of coral reef fishes. A thorough treatment of this complex subject is beyond
the scope of this chapter. For a more extensive discussion of social organization in
coral reef fishes, see Sale (1980a, pp. 379-387), Shapiro (1991) or Warner (1991).
Coral reef fishes that spend the majority of their time as truly solitary individuals
29
appear to be uncommon (personal observation). Many territorial fishes, which on first
impression appear to be solitary, are in fact clustered with other territorial individuals of
the same species and cannot therefor be considered "solitary" (see discussion below).
Perhaps the most common solitary fishes on Hawaiian coral reefs are roaming or siteattached piscivores like some jacks, trumpetfish, barracuda, sharks, etc. (personal
observation). In Hawaii, even these "solitary" species are often seen in twos or threes
(i.e. jacks). In other areas of the world these kinds of fishes (i.e. jacks, sharks,
barracuda) may occur in large aggregations or schools, depending upon species. In
summary, truly solitary fishes (i.e. individuals that do not regularly interact socially with
conspecifics) are relative uncommon on coral reefs.
A number of coral reef fishes occupy and defend territories. Territoriality is a
form of interference competition in which a defined space is defended on a temporary or
permanent basis for the purpose of securing some limiting resource. For coral reef
fishes, territorial boundaries contain food, shelter, spawning site, or a combination of
these factors (Shapiro 1991). Territoriality in coral reef fishes has been particularly well
studied in the damselfishes, but many other families like the butterflyfishes and
surgeonfishes have also received attention. Only a couple of representative examples
of fish territoriality will be mentioned here.
Low (1971), working on the Great Barrier Reef, conducted one of the first
comprehensive investigations of territoriality in a coral reef fish. He studied territorial
behavior in the damselfish, Pomacentrus flavicauda, a herbivorous species which
forages on filamentous algae growing on dead coral within its territorial boundaries.
This damselfish exhibited interspecific territorial defense, responding agonistically
toward 38 different species from 12 different families, while ignoring 16 other species
from 6 families. Thirty-five of the 38 species that were attacked were herbivores or
omnivores. The 16 species that were ignored were carnivores. The 3 carnivore
species attacked were large wrasses of the genus Choerodon which forage by
overturning coral boulders. These boulders are used by the damselfish for shelter and
for protection of eggs which are also laid on the territory. Low concluded that
territoriality in P. flavicauda was primarily a function of defense of food resources.
Tricas (1985), working in the reefs off Puako, Hawaii, studied space utilization in
the territorial brown-barred butterflyfish, Chaetodon multicinctus. Adults are
monogamous, obligate coral feeders (Reese 1975). Tricas discovered that this species
defends feeding territories against intrusion by conspecifics, other corallivorous
butterflyfishes like C. ornatissimus and C. quadrimaculatus, and even a corallivorous
damselfish (Plectroglyphidodon johnstonianus). Feeding territories at Puako averaged
about 57 m2 in area, were defended by a male/female pair, and shared contiguous
borders with other C. multicinctus territories that changed only slightly over the course
of a year. Pair fidelity was strong over the short term, and though usually not lasting
more than a year, at least one pair remained together in the same territory for more than
30
three years. The primary food resource defended by C. multicinctus at Puako was lobe
coral, Porites lobata, which comprised about 70% of the fish's diet.
Territory boundaries are not always static in time and may change seasonally or
in response to different intruders. Myrberg and Thresher (1974) studied territorial
behavior in males of the herbivorous threespot damselfish, Eupomacentrus planifrons,
in the Florida Keys. They found that the level of aggressive response varied with the
species of intruder, with some species being attacked farther from the territory center
than others. Conspecifics were always attacked farthest from the territory core,
followed by congeners (members of the same genus), and finally noncongeners. In
addition, Myrberg and Thresher found a seasonal shift in attack radius (i.e. aggressive
intensity) for most species of intruder. For most species, attack radius increased from a
minimum in January to a maximum in April. This change corresponds to aspects of the
annual reproductive cycle in this species. Eggs are deposited in male territories and are
then defended by the resident male. Reproductive activity peaks in April and is at a
minimum in January, and agonistic behavior associated with egg defense reflects this
change in reproductive activity. The authors conclude that E. planifrons defends "serial"
territories which contain more than one limiting resource, in this case both food and
reproductive site, and whose area of defense varies depending upon species of intruder
and time of year.
Territory size may also change in response to changes in resource or population
density. How territory size changes in response to changes in these variables (i.e.
whether it expands or contracts) depends upon a number of life-history traits of the
species in question. This is a surprisingly complex theoretical subject, and to elaborate
upon it here would be inappropriate. For additional information on optimization of
territory size consult Brown (1964), Ebersole (1980), Harvey and Mace (1983), Hixon
(1980, 1987), Schoener (1983), Shapiro (1991), and Warner (1991).
There is a growing body of evidence to suggest that territorial coral reef fishes
cluster in aggregations, although few studies have been done in which territories have
been mapped over a large enough area to document clumping statistically (Shapiro
1991). However, Sadovy (1986 as cited by Shapiro 1991) mapped territories of the
Caribbean damselfish, Stegastes partitus, and was able to statistically document that
this species occupied territories that were aggregated in clusters. Sadovy also
discovered that members of some clusters did not interact behaviorally with members of
others, and referred to these discrete aggregations as "colonies".
Clustering of territories into "colonies" may confer a number of advantages to
colony members which were reviewed by Shapiro (1991). Members may gain
increased protection from predators since clustering reduces each individual's
probability of being consumed when a predator strikes. They may also gain increased
protection from interspecific food competitors because entry into each member's
31
territory is blocked in part the territories of other members of the colony. Distance and
time needed to find a mate is lessened by clustering, reducing the time that members
spend off their territory. This in turn reduces the time they are away from shelter and
exposed to predators. It also reduces the time in which food resources on the territory
are unprotected. Reduced food loss to competitors may allow individuals in colonies to
hold smaller, easier to defend, territories than they would if they were more isolated. In
addition, neighbors may form alliances to help defend each other's territory against
incursions from potential territorial usurpers.
Many nonterritorial species of coral reef fishes will form aggregations or schools.
The proximal stimulus for aggregation/schooling is usually social attraction, although
ultimately these grouping form in response to a localized resource like mates or food, or
in response to attacks by visual predators. Before proceeding, differences in the
structural and behavioral characteristics of aggregated and schooled fishes should be
briefly mentioned. An aggregation of fishes may consist of several different species.
Furthermore, individuals in the aggregation are often of different sizes and generally are
not all oriented in the same direction. Fishes in a school are usually all of the same
species, are similar in size, are generally oriented in the same direction, and swimming
in unison. Sometimes the term "unpolarized school" is applied to aggregating fishes,
while fishes meeting the criteria listed above for schooled fishes are said to be in a
"polarized school". The majority of coral reef fishes which group socially form
aggregations rather than schools.
Examples of aggregating nonterritorial coral reef fishes are too numerous to list.
Many fishes on the reef aggregate around food resources. As mentioned in the
previous section on trophic interactions, many herbivorous fishes aggregate in areas of
the reef where plant resources are most abundant. Likewise, diurnal planktivores form
aggregations at the reef's edge where currents bringing zooplankton to the reef are
strongest. These aggregations, which sometimes become schools, also confer some
additional advantages beyond access to needed resources. As mentioned earlier in the
trophic ecology section, schools and aggregations are effective anti-predatory
adaptations which reduce each individual's probability of being consumed by a
piscivore. In the case of herbivores like surgeonfishes, schooling/aggregating is also an
effective foraging strategy in regard to swamping the defense system of territorial
herbivores like damselfishes (Robertson et al. 1976). For example, when a solitary
manini (Acanthurus sandwicensis) enters the territory of a Pacific Gregory (Stegastes
fasciolatus), it will be immediately chased out and rarely manages to feed prior to
eviction. However, when a school of manini enter that same damselfish's territory,
some individuals manage to feed while the damselfish is busy chasing others out of its
territory.
Not all aggregations of coral reef fishes center around food resources. In the
bluehead wrasse (Thalassoma bifasciatum), a species where protogynous
32
hermaphroditism is common, females may aggregate around solitary males for the
purpose of breeding. Before discussing aggregating behavior of the bluehead wrasse,
a brief review of sequential hermaphroditism is appropriate. A sequential
hermaphrodite is a fish which starts out life as one sex and later changes
morphologically and behaviorally to become the opposite sex (in spite of these changes
their genetic sex does not change). Fishes which start out life as females and change
sex to become males are called protogynous hermaphrodites. This is probably the
most common type of sequential hermaphroditism in fishes and is frequently seen in the
labrids, scarids, and serranids. Fishes which start out life as males and change sex to
become females are called protandrous hermaphrodites. This is apparently a rarer
phenomenon in the fishes but has been reported in a number of families including the
Gonostomatidae or bristlemouths, Serranidae or sea basses, Sparidae or porgies,
Centracanthidae - no common name, Labridae or wrasses, and Playtcephalidae or
flatheads (Bond 1979). For a theoretical analysis of hermaphroditism among animals
see Ghiselin (1969). For more information on sequential hermaphroditism in fishes
consult the numerous publications of Robert R. Warner (for a sampling see Warner et
al. 1975; Warner 1975, 1988a,b, 1991) and Douglas Y. Shapiro (for a sampling see
Shapiro 1979, 1980, 1984, 1987, 1989, 1991).
Returning to the bluehead wrasse, large males set up and defend mating
territories on elevated portions of the downcurrent edge of the reef (Warner 1991).
These territories serve as "egg-launching" sites for the species' pelagic eggs. Females
spend most of their time feeding upcurrent of the male breeding sites, but when they are
ready to mate, they migrate to a mating site, spawn, and then return to the feeding area
(Warner 1991). Females frequently arrive in sufficiently large numbers that groups of
them await their turn to spawn with a male. In addition, some mating sites are not
defended by a solitary male, but are instead occupied but not defended by groups of
smaller males. These aggregations of small males mate in groups with arriving females
(Warner et al. 1975). Basically, in the bluehead wrasse, either females or males may
form nonterritorial aggregations around reproductive resources (i.e. the opposite sex).
Before concluding, it is important to realize that for most species, social
organization or spacing patterns will change ontogenetically (Helfman 1978, Shapiro
1991). The mode of spacing utilized will therefor change depending upon the life history
stage of the species in question or even upon time of day (i.e. postlarvae, early stage
juvenile, late stage juvenile, adult). Shapiro (1991), in a review of intraspecific variability
in coral reef fish social systems, provides a number of examples of this ontogenetic
variation in social organization. One example concerned the French grunt, Haemulon
flavolineatum, in the Caribbean. Immediately after recruiting from the plankton, the
smallest postlarvae form mixed schools with mysid shrimps hovering near the bottom
over sea urchins or corals. Slightly larger juveniles form size-specific schools
associated with particular coral heads. Size uniformity in school members is thought to
increase locomotor efficiency and reduce the risk of predation. Large juveniles are
33
territorial, defending small territories over crevices or coral heads. Territories are also
thought to provide protection from predators. At night, all individuals migrate off the reef
to feed at nearby sea grass beds.
Another example of ontogenetic sequencing of social structure reviewed by
Shapiro concerns the protogynous redband parrotfish, Sparisoma aurofrenatum, of the
Caribbean (Clavijo 1982 as cited by Shapiro 1991). Individuals mature as females
which reside in territories of males where most reproduction occurs. Later in life
females leave the territories, wander briefly as females, change sex, and then wander
as males. Eventually these wandering males occupy a territory, and then spawn with
females in that territory. Individuals apparently shift from occupying territories to
wandering at the onset of sex change because newly sex-changed males improve their
reproductive output by locating vacant territories already containing two to five females
rather than remaining in their original territory to compete for females with the resident
male who is much larger. In summary, social structure in the redband parrotfish is
ontogenetically determined and is reflected in three patterns of space use: occupying
territories as juveniles and young adult females, wandering as females and then as
males, and finally re-occupying territories as males.
Community Structure of Coral Reef Fishes
Coral reef communities harbor extremely diverse fish assemblages which, near
the Indo-west Pacific center of tropical diversity, may number in the thousands of
species (Briggs 1974, Ebeling and Hixon 1991). How this high diversity is maintained
has been the source of considerable, and long-standing, debate (Hixon 1991). At the
most fundamental level, there are two basic views on how assemblages of competing
species on coral reefs might be organized. Those perspectives have been referred to
as the "equilibrium" and "nonequilibrium" views of community structure (see Connell
1978).
In the equilibrium view, species composition is a consequence of past and
present interspecific competition (i.e. competition between different species).
Interspecific competition is thought to result in a situation in which each species
occupies space or consumes food resources for which it is the most effective competitor
(Connell 1978). If there is no environmental perturbation, species composition of the
community persists through time; if perturbation occurs, community composition is
restored, through competition, to its original state (Connell 1978). In the nonequilibrium
view, natural disturbance and environmental change disrupt communities, often in an
abrupt and unpredictable manner (Connell 1978). Proponents of this view postulate
that the frequency of natural perturbation is sufficiently high that communities rarely fully
recover (reach "equilibrium") before more disturbance occurs. Because "equilibrium" is
rarely attained, competitively subordinate species are not inexorably excluded from the
34
community (Connell 1978).
On the coral reef, myriads of fish species with very similar resource requirements
seem to coexist in stark contrast to predictions based on equilibrium theory. This has
troubled fish biologists and community ecologists for almost two decades and has lead
to the formulation of a number of opposing hypotheses postulated to explain the high
diversity of tropical reef fishes. Generally, the hypotheses concerning coral reef fish
community structure fit into one of four basic models (Jones 1991): 1) the Competition
model, 2) the Lottery model, 3) the Predation-Disturbance model, and 4) the
Recruitment-Limitation model (for an alternate, though related, listing and discussion of
hypotheses concerning the community structure of coral and temperate reef fishes, see
Ebeling and Hixon 1991, pp 537-560). The Competition model falls within the
equilibrium view of community structure, while the remaining three models are all
variants of the nonequilibrium view. Each model is discussed in more detail below.
Competition Model
The Competition model, essentially synonymous with the equilibrium view of
community structure, assumes that the number and type of fish species found on coral
reefs is determined through competition for limited resources (Smith and Tyler 1972,
Smith 1978). As pointed out by Ebeling and Hixon (1991), in their review of tropical and
temperate fish communities, this "niche diversification" model has two versions. The
first proposes that as a result of competition for limited resources over evolutionary time,
coral reef fishes have become resource specialists and competitive exclusion is
prevented. The second assumes that competition is currently occurring among fishes
occupying coral reefs. Competitive exclusion doesn't occur because the environment
either provides resource refuges for subordinate competitors (i.e. a suboptimal area or
food items not preferred by the dominant competitor and hence available to the
subordinate) or because each competitor is dominant in a particular subhabitat or in
regard to utilizing some subsection of a resource base like food. In either case, coral
reef fishes should exhibit some form of "resource partitioning" like eating different arrays
of prey, residing and/or foraging on different parts of the reef, or being active at different
times of day (Ebeling and Hixon 1991).
The competition or niche diversification model postulates that the high species
diversity exhibited by fishes in coral reef ecosystems is attributable to an abundance of
species which utilize narrow and finely partitioned niches (i.e. that it is because of finegrained resource partitioning which is ultimately attributable to competition) (Mead 1970,
Briggs 1974, Ebeling and Hixon 1991). There is considerable evidence to suggest that
resource partitioning does occur widely among fishes inhabiting coral reef
environments. Of 38 investigations cited by Ebeling and Hixon (1991) which
investigated possible resource partitioning by tropical marine fishes, 82% found
evidence of resource partitioning (see pp. 539-542 of Ebeling and Hixon for a tabular
35
summary results from studies cited). The resources most commonly "partitioned" are
habitat or food, although temporal partitioning has also been described (Hobson 1972,
Collette and Talbot 1972, Domm and Domm 1973).
The common occurrence of resource partitioning among coral reef fishes
suggests that the competition or niche diversification model has merit. However,
caution may be advised. Citing Ross (1986), Ebeling and Hixon warned that resource
partitioning may simply reflect chance divergences in the evolutionary histories of the
species involved and may have nothing to do with competition. Peter Sale remarked:
"Given that three species of fish on a reef will inevitably differ in some aspect of what
they do, how useful is a triumphant documentation of resource partitioning anyway?"
(personal communication cited by Ebeling and Hixon 1991). That coral reef fishes
partition resources on the reef is irrefutable. Whether that partitioning is always
indicative of underlying competition for limited resources remains a source of contention
among coral reef ecologists.
Lottery Model
The Lottery model, the first to deviate from traditional ecological thought,
maintains that chance recruitment of fishes to the reef and their subsequent ability to
competitively hold onto limited space determines species composition on the reef (Sale
1974, 1977, 1978, 1991c; Sale and Dybdahl 1975). Sale (1974), in studying
ecologically similar and co-occurring territorial damselfishes on the Great Barrier Reef,
concluded that although there was some evidence of partitioning of food and habitat
among the damselfishes, resource utilization by the fishes exhibited great overlap.
Furthermore, removal of individuals produced major changes in territorial boundaries
and species composition which persisted through time. Sale concluded that
coexistence among the damselfishes, "appears to be maintained primarily because
recruitment of juveniles is an essentially chance process depending upon (a) the
random creation of vacant living space, and (b) the uncontrolled dispersal of the pelagic
larvae."
Sale and Dybdahl (1975), in another investigation on the Great Barrier Reef, did
successive collections of all fishes occupying replicate heads of living and dead coral
(dubbed "L-units" and "D-units" by the authors) approximately every four months over a
period of about two years. They discovered that the living and dead coral units were
remarkably similar in regard to the composition of fishes collected from them (i.e.
relatively few species exhibited a strong preference for L or D units). They also
discovered that for any specific coral head, the assemblages of fish species captured on
successive collections could be quite different from collection to collection.
Sale and Dybdahl's results didn't fit the equilibrium view of community structure
which would have predicted very different species assemblages for live and dead units
36
(i.e. resource partitioning of very different habitat types), and would have predicted that
specific units would be repeatedly occupied by similar assemblages of species (i.e.
predictable recruitment of species based on resource needs matching those available in
the vacated coral heads). While acknowledging that on a large scale fishes may
partition their habitat spatially, they concluded that on a small scale the distribution of
species reoccupying vacated coral heads was the result of chance colonization, not of a
systematic partitioning of living space. Once a coral head is fully filled with colonists,
those fish successfully hold onto that space until they die or are removed by some form
of disturbance.
Since those early pioneering reports, Sale has written many articles which
elaborate upon and refine the Lottery model (Sale 1977, 1978, 1979, 1980a&b, 1985,
1991c). Nonetheless the core of the original hypothesis remains intact; coral reef fish
community structure is determined largely by chance recruitment of larval fishes onto
patches of newly-vacated and limiting space on the reef. These communities are "open
nonequilibrial systems" in which reef fish species exist in spatially divided populations in
a patchy environment (Sale 1991c, Mapstone and Fowler 1988). Local populations
export all gametes/larvae to the open ocean and receive new recruits from the open
ocean, almost certainly recruits produced by other populations (Sale 1991c). Local
recruitment of each species is therefor independent of local reproductive success,
relying instead on success of other populations. Sale (1991c) points out that the
decoupling of reproduction and subsequent recruitment "means that even strong
interspecific competition among local residents cannot lead to permanent local
extinction, nor to a coevolved partitioning of resources in the manner predicted by
classical competition theory." High larval mortality during the planktonic phase can add
to the unpredictability of larval recruitment onto the reef and may ultimately lead to
change in community structure (Sale 1991c, Jones 1991).
In conclusion, reef fish compete with each other through their planktonic larvae to
obtain limiting resources which are both patchy in distribution and unpredictably
available. Diversity of fishes on the reef is high because species with highly overlapping
resource requirements coexist, not through resource partitioning, but rather by recruiting
to and holding small patches of space on the reef. In this regard, the reef might be
viewed as a patch-work quilt of stochastically recruited species assemblages.
Predation Disturbance Model
The Predation-Disturbance model assumes that adult populations are held below
the level at which resources become limiting through postsettlement mortality of
juveniles and adults from predation and that competitive exclusion therefor does not
occur (Goldman and Talbot 1976; Johannes 1978; Talbot et al. 1978; Bohnsack and
Talbot 1980; Hixon and Beets 1989, 1993; Hixon 1991). This hypothesis has not
received as much attention as some of the others which, according to Hixon (1991), is
37
surprising given the attention predation has received in behavioral and community
ecology and in marine fisheries biology.
Hixon (1991), in a review and analysis of predation's role in structuring coral reef
fish communities, points out that the predation hypothesis has generated two basic
predictions. First, if predation is important, prey fishes should be morphologically and
behaviorally adapted to minimize the risk of predation. Second, the abundance of prey
species should shift predictably when the density of predators or prey refuges changes.
The first prediction appears to be substantiated by the diverse anti-predatory
adaptations that have evolved among prey fishes, as well by the ubiquity of piscivores
on the reef and their own adaptations for successfully securing prey. The wide array of
predator and prey adaptations (morphological, chemical, and behavioral) among reef
fishes were discussed previously in the "Carnivores" subsection of the Trophic Ecology
section of this chapter. Although evolutionary evidence is indirect or circumstantial it
nonetheless suggests that predation is indeed a significant force structuring coral reef
fish communities (Hixon 1991).
The second prediction is also supported by the results of numerous
investigations. On the Great Barrier Reef, Thresher (1983a) reported a significant
inverse correlation between the abundance of the piscivorous serranid Plectropomus
leopardus and the abundance of a number of diurnal planktivores (the pomacentrid
Acanthochromis polyacanthus and four cardinalfishes). Furthermore, over the course of
a year, adult Acanthochromis disappeared on 3 of 4 reefs where the serranid was
present, but disappeared on only 1 of 20 reefs where Plectropomus was absent
(Thresher 1983b). In the Caribbean, Shulman et al. (1983) followed colonization of
replicate artificial habitats by predator and prey fishes and found that on reefs having
early immigration of snappers (Lutjanus spp.) subsequent colonization of grunts
(Haemulon and Equetus spp.) was significantly lower than on habitats where the
snappers were absent.
Hixon and Beets (1989), working in the Virgin Islands, evaluated the effects of
various hole numbers and sizes on fish assemblages colonizing concrete-block reefs.
They found that reefs with more holes supported more fishes and that the size of fishes
on reefs was correlated to hole size (i. e. reefs with small holes supported more small
fishes and reefs with large holes supported more large fishes). These results suggest
that appropriate sized holes (which probably serve as refugia from predators) are an
important factor in determining community structure of tropical reef fishes. During that
study, Hixon and Beets also detected a significant negative correlation between the
number of resident piscivores and the maximum number of potential prey fish occupying
a reef, and concluded that piscivores probably set the upper limit to the number of small
fishes that can occupy a reef.
38
Hixon and Beets (1993), again working in the Virgin Islands with concrete-block
reefs, conducted manipulations designed to test a number of hypotheses regarding the
role of predation in structuring reef-fish assemblages. As in their earlier investigation
(1989), they 1) found a positive correlation between the number of holes available and
prey abundance, although the results were complicated somewhat at higher hole
densities by a temporary over-saturation of the study area with holes, and 2) they
discovered that the maximum number of reef-associated prey fishes declined
significantly with increasing predator abundance. Among their new discoveries, they
found that prey fishes were most abundant on reefs with holes approximating their body
diameter, presumedly because these holes afforded maximum protection from
predators. Finally, they observed a significant negative correlation between predator
abundance and the maximum number of prey species observed (i.e. prey species
richness), and concluded that piscivores have a negative effect on prey species
diversity by nonselectively reducing and sometimes eliminating both common and rare
species (see also Hixon 1991, pp 492-493).
In conclusion, predation is a process that appears to contribute to the structuring
of reef fish communities by causing mortality at all stages in the life history of every fish
species. According to Hixon and Beets (1993), even if fishes undergo recruitment
limitation (covered next), predation can force prey fishes to compete for refuge holes
and can affect local species diversity by altering the distribution and abundances of prey
species.
Recruitment Limitation Model
The Recruitment-Limitation model, the newest and perhaps most widely
accepted model, maintains that larval recruitment is usually too low for adult populations
to ever reach the "carrying capacity" of the reef environment, so resources are not
limiting and competitive exclusion therefor does not occur (Williams 1980, Doherty
1981, Victor 1983, Doherty and Williams 1988). A correlate to this is that population
density and age structure should simply reflect variations in input of recruits, and should
be not be strongly effected by postrecruitment processes like competition (Jones 1991).
Williams (1980) studied assemblages of about eight species of pomacentrid on
small patch reefs in One Tree Lagoon on the Great Barrier Reef and discovered that
resident populations of damselfish did not significantly affect recruitment of
pomacentrids to the patch reefs. Williams found some site selection by settling
juveniles, but selection was not influenced by the number of pomacentrids on the reef.
He also found that over the course of the two and a half year study, the total number of
pomacentrids on patch reefs fluctuated greatly. He concluded that the number of fish
on any given reef was primarily dependent upon the number of larvae present in the
plankton, habitat selection by larvae, and post-settlement predation, but that it was
independent of competitive interactions among resident damselfishes.
39
Doherty (1981) questioned whether marine fishes regularly saturate reef habitats
with more juvenile fishes than they can absorb thereby activating compensatory
mechanisms (i.e. activating density-dependent population regulating mechanisms)
whereby colonists fail to recruit to the reef or suffer high mortality after settlement. If
they do, the magnitude of recruitment or the survival of post-recruitment juveniles
should be inversely correlated to the density of resident adults in the habitat. In a study
of the herbivorous damselfish, Pomacentrus wardi, on the Great Barrier Reef, Doherty
(1981) compared field densities of this fish to computer-generated densities for a
population based on random recruitment and density-independent mortality, and found
that they could not be distinguished from each other. He concluded that this species is
not normally subject to density regulation.
Victor (1983) studied recruitment and population dynamics of the bluehead
wrasse (Thalassoma bifasciatum) in the eastern Pacific, off Panama. He was able to
determine that recruitment occurs in short and sporadic episodes, in spite of the fact
that adults spawn every day. Recruitment episodes of juveniles to the reef were not
effected by resident wrasse densities on the reef, suggesting that competition with
residents was not a factor affecting recruitment in this species. By monitoring the age
structure of wrasses on a single patch reef, Victor was able to determine that the
composition of the adult population directly reflected the recruitment of juveniles to the
reef the year before, and was subject to dramatic fluctuations in size from year to year.
He concluded that the population dynamics of the blue head wrasse were determined
by the supply of recruits during the previous year and not by competition for space or
some other resource on the reef.
In conclusion, coral reef fish populations as envisioned by the recruitmentlimitation model are strongly influenced by fluctuations in recruitment and these
fluctuations are preserved in the age structure of the populations (Doherty and Williams
1988). Larval recruitment levels are thought to be insufficient to saturate the coral reef
environment, resources are never fully utilized, and competition is therefore not thought
to be an important factor in regard to structuring of fish assemblages on coral reefs. In
essence, density-independent and highly variable recruitment determines patterns of
abundances of species and hence the population structure of assemblages of species.
As summarized by Mapstone and Fowler (1988): "The species composition and relative
numbers of fish present will be determined only by recruitment of planktonic larvae and
larval habitat selection. Reef fish assemblages are, therefore, intrinsically very variable
in space and time, with population densities and species composition being inconstant"
(p. 73). For a comprehensive review of investigations supporting this model see
Mapstone and Fowler (1988), Doherty and Williams (1988), and Doherty (1991).
Summary
40
Which of these models is correct remains to be determined. Although there are
investigations which support each model, much current evident supports the
Recruitment Limitation Model and that model probably has the most advocates at this
time (see Doherty and Williams 1988). However, Hixon (1991) makes a convincing
argument that many of these models are not necessarily mutually exclusive and that
there is considerable common ground for a synthesis. Nonetheless, until more work
has been done, the structuring of tropical coral reef fish communities will probably
remain a source of contention among ichthyologists and marine ecologists. For a
recent and coordinated series of reviews of tropical reef fish community organization
see Ebeling and Hixon (1991), Hixon (1991), Jones (1991), Sale (1991c), Thresher
(1991), and Williams (1991).
41
References
Allen, G. R. 1981. Butterfly and Angelfishes of the World, Vol. 2. Mergus, Melle,
Germany.
Aronson, R. B. 1983. Foraging behavior of the west Atlantic trumpetfish, Aulostomus
maculatus: Use of large, herbivorous reef fishes as camouflage. Bull. Mar. Sci. 33:166171.
Bakun, A. 1986. Local retention of planktonic early life stages in tropical reef/bank
demersal systems: The role of vertically-structured hydrodynamic processes. In
"IOC/FAO Workshop on Recruitment in Tropical Coastal Demersal Communities," (D.
Pauly and A. Yanez-Arancibia, eds.), IOC Workshop Rep. 44 (suppl.), pp. 15-32.
UNESCO, Paris.
Bakus, G. J. 1964. The effects of fish-grazing on invertebrate evolution in shallow
tropical waters. Allan Hancock Found. Publ. 27:1-29.
Bakus, G. J. 1966. Some relationships of fishes to benthic organisms on coral reefs.
Nature (London) 210:280-284.
Bakus, G. J. 1969. Energetics and feeding in shallow marine waters. Int. Rev. Gen.
Exp. Zool. 4:273-369.
Bakus, G. J. 1981. Chemical defense mechanisms on the Great Barrier Reef, Australia.
Science 211:497-499.
Bakus, G. J. 1983. The role of fishes in the structuring of coral reef communities.
Proceedings of the International Conference on Marine Science in the Red Sea. Bull.
Egypt. Inst. Oceanogr. Fish. 9:186-192.
Bakus, G. J., and G. Green 1974. Toxicity in sponges and holothurians: A geographic
pattern. Science 185:951-953.
Bardach, J. E., H. E. Winn and D. W. Menzel 1959. The role of senses in the feeding of
the nocturnal reef predators Gymnothorax moringa and G. vivinus. Copeia 1959:133139.
Barlow, G. W. 1981. Patterns of parental investment, dispersal and size among coralreef fishes. Environ. Biol. Fishes 6:65-85.
Bellwood, D. R., and J. H. Choat 1989. A description of the juvenile phase colour
patterns of 24 parrotfish species (family Scaridae) from the Great Barrier Reef,
41
Australia. Rec. Aust. Mus. 41:1-41.
Bertness, M. D. 1981. Predation, physical stress, and the organization of a tropical
rocky intertidal hermit crab community. Ecology 62:411-425.
Bohnsack, J. A., and Talbot, F. H. 1980. Species packing by reef fishes on Australian
and Caribbean reefs: An experimental approach. Bull. Mar. Sci. 30:710-723.
Bond, C. E. 1979. Biology of Fishes. W. B. Saunders Company, Philadelphia, 514 pp.
Bourret, P., D. Binet, C. Hoffschir, J. Rivaton and H. Velayoudon 1979. "Evaluation de
'l' effet d'ile' d'un atoll: Plancton et micronecton au large de Mururoa (Tuamotus)." Cent.
ORSTOM Noumea, New Caledonia, French Polynesia.
Bowen, S. H. 1979. A nutritional constraint in detritivory by fishes: the stunted
population of Sarotherodon mossambicus in Lake Sibaya, South Africa. Ecol. Monogr.
47:17-31.
Bray, R. N., A. C. Miller, and G. G. Geesey 1981. The fish connection: A trophic link
between planktonic and rocky reef communities. Science 214:204-205.
Briggs, J. C. 1974. Marine Zoogeography. McGraw-Hill, New York, 475 pp.
Brock, R. E., C. Lewis and R. C. Wass 1979. Stability and structure of a fish community
on a coral patch reef in Hawaii. Mar. Biol. 54:281-292.
Brothers, E. B., D. M. Williams and P. F. Sale 1983. Length of larval life in twelve
families of fishes at "One Tree Lagoon", Great Barrier Reef, Australia. Mar. Biol.
76:319-324
Brothers, E. B. and R. E. Thresher 1985. Pelagic duration, dispersal, and the
distribution of Indo-Pacific coral-reef fishes. In "The Ecology of Coral Reefs" (M. L.
Reaka, ed.), NOAA Symp. Ser. Undersea Res., Vol. 3, pp. 53-69. Natl. Oceanic Atmos.
Adm., Rockville, Maryland.
Brown, J. L. 1964. The evolution of diversity in avian territorial systems. Wilson Bull.
76:293-329.
Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal
communities. Ecol. Monogr. 56:345-363.
Carroll, R. L. 1987. Vertebrate paleontology and evolution. Freeman, New York.
42
Choat, J. H. 1968. Feeding habits and distribution of Plectropomus maculatus
(Serraidae) at Heron Island. Proc. R. Soc. Queensl. 80:13-18.
Choat, J. H. 1991. The biology of herbivorous fishes on coral reefs. Pgs 120-155 in P.
F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA,
92101, 754 pp.
Choat, J. H., and D. R. Bellwood 1991. Reef fishes: their history and evolution. Pgs 3966 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San
Diego, CA, 92101, 754 pp.
Clavijo, I. 1982. Aspects of the reproductive biology of the redband parrotfish
Sparisoma aurofrenatum. Unpublished Ph.D. thesis, University of Puerto Rico,
Mayaguez, Puerto Rico.
Clements, K. D., D. C. Sutton and J. H. Choat 1989. Occurrence and characteristics of
unusual protistan symbionts from surgeon fishes (Acanthuridae) of the Great Barrier
Reef, Australia. Mar. Biol. 102:403-412.
Cohen, D. M. 1970. How many recent fishes are there? Proc. Calif. Acad. Sci. 37:341346.
Collettee, B. B., and F. H. Talbot 1972. Activity patterns of coral reef fishes with
emphasis on nocturnal-diurnal changeover. Bull. Nat. Hist. Mus. Los Angeles County
14:98-124.
Compagno, L. J. V. 1973. Interrelationships of living elasmobranchs. Pgs 15-62 in P.
H. Greenwood, R. S. Miles, and C. Patterson, eds. Interrelationships of fishes. New
York: Academic Press.
Compagno, L. J. V. 1977. Phyletic relationships of living sharks and rays. Amer. Zool.
17:303-322.
Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science
199:1302-1310.
Cox, E. F. 1986. The effects of a selective corallivore on growth rates and competition
for space between two species of Hawaiian corals. J. Exp. Mar. Biol. Ecol. 101:161174.
Davis, W. P. and R. S. Birdsong 1973. Coral reef fishes which forage in the water
column. Helgol. Wiss. Meeresunters. 24:292-306.
43
Day, R. W. 1977. Two contrasting effects of predation on species richness in coral reef
habitats. Mar. Biol. 44:1-5.
Day, R. W. 1985. The effects of refuges from predators and competitors on sessile
communities on a coral reef. Proc. Int. Coral Reef Congr., 5th 4:41-45.
Doherty, P. J. 1981. Coral reef fishes: Recruitment-limited assemblages? Proc. Int.
Coral Reef Symp., 4th 2:465-470.
Doherty, P. J. 1991. Spatial and temporal patterns in recruitment. Pgs 261-293 in P. F.
Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA,
92101, 754 pp.
Doherty, P. J., D. McB. Williams and P. F. Sale 1985. The adaptive significance of
larval dispersal in coral reef fishes. Environ. Biol. Fishes 12:81-90.
Doherty, P. J., and D. McB. Williams 1988. The replenishment of coral reef fish
populations. Oceanogr. Mar. Biol. 26:487-551.
Domm, S. B., and A. J. Domm 1973. The sequence of appearance at dawn and
disappearance at dusk of some coral reef fishes. Pac. Sci. 27:128-135.
Earle, S. A. 1972. The influence of herbivores on the marine plants of Great Lameshur
Bay, with an annotated list of plants. Natur. Hist. Mus. L.A. County, Ca. Sci. Bull. 14:1744.
Ebeling, A. W., and M. A. Hixon 1991. Tropical and temperate reef fishes: comparison
of community structures. Pgs 509-563 in P. F. Sale, ed. The Ecology of Fishes on
Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Ebersole, J. P. 1980. Food density and territory size: An alternative model and a test on
the reef fish Eupomacentrus leucostictus. Am. Nat. 115:492-509.
Emery, A. R. 1968. Preliminary observations on coral reef plankton. Limnol. Oceanogr.
13:293-303.
Fagerstrom, J. A. 1987. The Evolution of Reef Communities. Wiley, New York.
Finucane, J. H., C. B. Grimes and S. P. Naughton 1991. Diets of young king and
Spanish mackerel off the southeast United States. Northeast Gulf Science 11:145-153.
Fishelson, L., W. L. Montgomery and A. A. Myrberg 1985. A unique symbiosis in the
gut of tropical herbivorous surgeon fish (Acanthuridae: Teleostei) from the Red Sea.
44
Science 229:49-51.
Gaines, S. D., and J. Lubchenco 1982. A unified approach to marine plant-herbivore
interactions: II. Biogeography. Annu. Rev. Ecol. Syst. 13:111-138.
Ghiselin, M. T. 1969. The evolution of hermaphroditism among animals. Q. Rev. Biol.
44:189-208.
Gladfelter, W. B. 1979. Twilight migrations and foraging activities of the copper
sweeper Pempheris schomburgki (Teleostei: Pempheridae). Mar. Biol. 50:109-119.
Gladstone, W. 1987. The eggs and larvae of the sharpnose pufferfish Canthigaster
valentini (Pisces: Tetraodontidae) are unpalatable to other reef fishes. Copeia
1987:227-230.
Glynn, P. W. 1988. Predation on coral reefs: Some key processes, concepts and
research directions. Proc. Int. Coral Reef Symp., 6th 1:51-62.
Glynn, P. W. 1990. Feeding ecology of selected coral-reef macroconsumers: patterns
and effects on coral community structure. Pp. 365-400 [In] Dubinsky, Z. (Editor).
Ecosystems of The World 25: Coral Reefs. Elsevier, 550 pp.
Goldman, B. and F. H. Talbot 1976. Aspects of the ecology of coral reef fishes. Pp.
125-154 [In] Jones, O. A. and R. Endean (Editors). Biology and Geology of Coral
Reefs, Vol 3. Academic Press, New York, ___ pp.
Gosline, W. A. 1971. Functional morphology and classification of teleostean fishes.
Press University of Hawaii, Honolulu, 208 pp.
Gray, C. A. 1993. Horizontal and vertical trends in the distributions of larval fishes in
coastal waters off New South Wales, Australia. Mar. Biol. 116:649-666.
Green, G. 1977. Ecology of toxicity in marine sponges. Mar. Biol. 40:207-215.
Guzman, H. M., and D. R. Robertson 1989. Population and feeding responses of the
corallivorous pufferfish Arothron meleagris to coral mortality in the eastern Pacific. Mar.
Ecol. Prog. Ser. 55:121-131.
Halstead, B. W. 1978. Poisonous and Venomous Marine Animals of the World. Darwin,
Princeton, New Jersey.
Hamilton, W. D. 1971. Geometry for the selfish herd. Journal Theor. Biol. 31:295-311.
45
Harmelin-Vivien, M. L. 1981. Trophic relationships of reef fishes in Tulear
(Madagascar). Oceanol. Acta 3:365-374.
Harmelin-Vivien, M. L., and C. Bouchon 1976. Feeding behavior of some carnivorous
fishes (Serranidae and Scorpaenidae) from Tulear (Madagascar). Mar. Biol. 37:329340.
Hartline, A. C., P. H. Hartline, A. M. Szmant, and A. O. Flechsig 1972. Escape
response in a pomacentrid reef fish, Chromis cyaneus. Bull. Nat. Hist. Mus. Los
Angeles County 14:93-97.
Harvey, P. H. and G. M. Mace 1983. Foraging models and territory size. Nature
(London) 305:14-15.
Hay, M. E. 1991. Fish-seaweed interactions on coral reefs: effects of herbivorous fishes
and adaptations of their prey. Pgs 96-119 in P. F. Sale, ed. The Ecology of Fishes on
Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Helfman, G. S. 1978. Patterns of community structure in fishes: Summary and
overview. Environ. Biol. Fishes 3:129-148.
Hiatt, R. W., and D. W. Strasburg 1960. Ecological relationships of the fish fauna on
coral reefs of the Marshall Islands. Ecol. Monogr. 30:65-127.
Hixon, M. A. 1980. Food production and competitor density as the determinants of
feeding territory size. Am. Nat. 115:510-530
Hixon, M. A. 1987. Territory area as a determinant of mating systems. Am. Zool.
27:229-247.
Hixon, M. A. 1991. Predation as a process structuring coral reef fish communities. Pgs
475-508 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San
Diego, CA, 92101, 754 pp.
Hixon, M. A. and J. P. Beets 1989. Shelter characteristics and Caribbean fish
assemblages: Experiments with artificial reefs. Bull. Mar. Sci. 44:666-680.
Hixon, M. A. and J. P. Beets 1993. Predation, prey refuges, and the structure of coralreef fish assemblages. Ecol. Monogr. 63:77-101.
Hobson, E. S. 1968. Predatory behavior of some shore fishes in the Gulf of California.
46
Res. Rep. - U. S. Fish Wildl. Serv. 73:1-92.
Hobson, E. S. 1972. Activity of Hawaiian reef fishes during the evening and morning
transitions between daylight and darkness. Fish. Bull. 70:715-740.
Hobson, E. S. 1974. Feeding relationships of teleostean fishes on coral reefs in Kona,
Hawaii. Fish. Bull. 72:915-1031.
Hobson, E. S. 1975. Feeding patterns among tropical reef fishes. Am. Sci. 63:382-392.
Hobson, E. S. 1979. Interactions between piscivorous fishes and their prey. In
"Predator-Prey Systems in Fisheries Management" (H. E. Clepper, ed.), pp. 231-242.
Sport Fishing Inst., Washington, D. C.
Hobson, E. S. 1991. Trophic relationships of fishes specialized to feed on zooplankters
above coral reefs. Pgs 69-95 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs.
Academic Press, San Diego, CA, 92101, 754 pp.
Hobson, E. S. and E. H. Chave 1990. Hawaiian Reef Animals, Revised Edition.
University of Hawaii Press, Honolulu, Hawaii, 137 pp.
Hobson, E. S. and J. R. Chess 1978. Trophic relationships among fishes and plankton
in the lagoon at Enewetak Atoll, Marshall Islands. Fish. Bull. 76:133-153.
Hobson, E. S. and J. R. Chess 1986. Diel movements of resident and transient
zooplankters above lagoon reefs at Enewetak Atoll, Marshall Islands. Pac. Sci. 40:7-26.
Horn, M. H. 1989. Biology of marine herbivorous fishes. Oceanogr. Mar. Biol. 27:167272.
Houde, E. D. and J. A. Lovdal 1984. Seasonality of occurrence, foods and food
preferences of ichthyoplankton in Biscayne Bay, Florida. Estuarine, Coastal Shelf Sci.
20:79-103.
Hourigan, T. F. and E. S. Reese 1987. Mid-ocean isolation and the evolution of
Hawaiian reef fishes. Trends Ecol. Evol. 2:187-191.
Hunter, J. R. 1984. Inferences regarding predation on the early life stages of cod and
other fishes. Flodevigen Rapp. 1:533-562.
Hutchings, P. A. 1986. Biological destruction of coral reefs. A review. Coral Reefs
4:239-252.
47
Jenkins, G. P., N. E. Milward and R. F. Hartwick 1984. Food of larvae of Spanish
mackerels, genus Scomberomorus (Teleostei: Scombridae), in shelf waters of the Great
Barrier Reef. Aust. J. Mar. Freshwater Res. 35:477-482.
Johannes, R. E. 1978. Reproductive strategies of coastal marine fishes in the tropics.
Environ. Biol. Fishes 3:65-84.
Johannes, R. E. 1981. Words of the Lagoon: Fishing and Marine Lore in the Palau
District of Micronesia. Univ. of California Press, Berkeley, California.
Jones, G. P. 1991. Postrecruitment processes in the ecology of coral reef fish
populations: a multifactorial perspective. Pgs 294-328 in P. F. Sale, ed. The Ecology of
Fishes on Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Jones, G. P., P. F. Sale and D. J. Ferrell 1988. Do large carnivorous fishes affect the
ecology of macrofauna in shallow lagoonal sediments?: A pilot experiment. Proc. Int.
Coral Reef Symp., 6th 2:77-82.
Jones, G. P., D. J. Ferrell and P. F. Sale 1991. Fish predation and its impact on the
invertebrates of coral reefs and adjacent sediments. Pgs 156-179 in P. F. Sale, ed. The
Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Kaufman, L. S. 1976. Feeding behavior and functional coloration of the Atlantic
trumpetfish, Aulostomus maculatus. Copeia 1976:377-378.
Kingsford, M. J. and J. H. Choat 1989. Horizontal distribution patterns of presettlement
reef fish: are they influenced by the proximity of reefs? Mar. Biol. 101:285-297.
Lachner, E. A. and S. J. Karnella 1980. Fishes of the Indo-Pacific genus Eviota with
descriptions of eight new species (Teleostei: Gobiidae). Smithson. Contrib. Zool. 315:1127.
Lagler, K. F., J. E. Bardach, R. R. Miller, and D. R. M. Passino 1977. Ichthyology, 2nd
Edition. John Wiley & Sons, New York, 506 pp.
Lang, J.C. and E.A. Chornesky 1990. Competition between scleractinian reef corals - a
review of mechanisms and effects. Pp. 209-252 [In] Dubinsky, Z. (Editor).
Leis, J. M. 1978. Systematics and zoogeography of the porcupinefishes (Diodon,
Diodontidae, Tetraodontiformes), with comments on egg and larval development. Fish.
Bull. 76:535-567.
48
Leis, J. M. 1982. Nearshore distributional gradients of larval fish (15 taxa) and
planktonic crustaceans (6 taxa) in Hawaii. Mar. Biol. 72:89-97.
Leis, J. M. 1986. Vertical and horizontal distribution of fish larvae near coral reefs at
Lizard Island, Great Barrier Reef. Mar. Biol. 90:505-516.
Leis, J. M. 1991a. The pelagic stage of reef fishes: the larval biology of coral reef
fishes. Pgs 183-230 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs.
Academic Press, San Diego, CA, 92101, 754 pp.
Leis, J. M. 1991b. Vertical distribution of fish larvae in the Great Barrier Reef Lagoon,
Australia. Mar. Biol. 109:157-166.
Lewis, S. M. 1986. The role of herbivorous fishes in the organization of a Caribbean
reef community. Ecol. Monogr. 56:183-200.
Liew, H.-C. 1983. Studies of flatfish larvae (Fam. Psettodidae, and Bothidae,
Pleuronectiformes) in the shelf waters of the central Great Barrier Reef, Australia.
Unpublished M.S. thesis, James Cook University, Townsville, Australia.
Littler, M. M., and D. S. Littler 1984. Models of tropical reef biogenesis. Prog. Phycol.
Res. 3:323-364.
Lobel, P. S. 1981. Trophic biology of herbivorous reef fishes: alimentary pH and
digestive capabilities. J. Fish. Biol. 19:365-397.
Lobel, P. S., and A. R. Robinson 1985. The potential role of ocean eddies in the life
histories of Hawaiian fishes. Spec. Publ.--Hawaii. Inst. Geophys. 1985:61-85.
Lobel, P. S., and A. R. Robinson 1986. Transport and entrapment of fish larvae by
ocean mesoscale eddies and currents in Hawaiian waters. Deep-Sea Res. 33:483-500.
Losey, G. S. 1972. Predation protection in the poison-fang blenny, Meiacanthus
atrodorsalis, and its mimics, Escenius bicolor and Runula laudadus (Blenniidae). Pac.
Sci. 26:129-139.
Low, R. M. 1971. Interspecific territoriality in a pomacentrid reef fish, Pomacentrus
flavicauda Whitley. Ecology 52:648-654.
Mapstone, B. D., and A. J. Fowler 1988. Recruitment and the structure of assemblages
of fish on coral reefs. Trends Ecol. Evol. 3:72-77.
49
Marshall, N. B. 1965. The Life of Fishes. Weidenfeld and Nicolson, London, 402 pp.
Mattson, W. J. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol.
Syst. 11:119-161.
McClanahan, T. R., and N. A. Muthiga 1989. Patterns of predation on a sea urchin,
Echinometra mathaei (de Blainville), on Kenyan coral reefs. J. Exp. Mar. Biol. Ecol.
126:77-94.
McClanahan, T. R., and S. H. Shafir 1990. Causes and consequences of sea urchin
abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362-370.
McCosker, J. E. 1977. Fright posture of the plesiopid fish Calloplesiops altivelis: An
example of Batesian mimicry. Science 197:400-401.
McFarland, W. N. 1985. Overview: the dynamics of recruitment in coral reef organisms.
In "The Ecology of Coral Reefs" (M.L. Reaka, ed.), NOAA Symp. Ser. Undersea Res.,
Vol. 3, pp. 9-15. Natl. Oceanic Atmos. Adm., Rockville, Maryland.
McFarland, W. N. 1991. The visual world of coral reef fishes. Pgs 16-38 in P. F. Sale,
ed. The Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA, 92101,
754 pp.
Mead, G. W. 1970. A history of South Pacific fishes. In "Scientific Exploration of the
South Pacific" (W. S. Wooster, ed.), pp. 236-251. Natl. Acad. Sci., Washington, D. C.
Moyle, P. B. and J. J. Cech, Jr. 1988. Fishes an Introduction to Ichthyology, 2nd.
Prentice Hall, Englewood Cliffs, New Jersey 07632, 559 pp.
Munz, F. W. and W. N. McFarland 1973. The significance of spectral position in the
rhodopsins of tropical marine fishes. Vision Res. 13:1829-1874.
Myers, R. F. 1989. "Micronesian Reef Fishes", Coral Graphics, Agana Guam.
Myrberg, A. A. and R. E. Thresher 1974. Interspecific aggression and its relevance to
the concept of territoriality in reef fishes. Am. Zool. 14:81-96.
Nelson, J. S. 1984. Fishes of the World, 2nd. Wiley-Interscience, John Wiley & Sons,
New York, 523 pp.
Neudecker, S. 1977. Transplant experiments to test the effect of fish grazing on coral
distribution. Proc. Int. Coral Reef Symp., 3rd 1:318-323.
50
Neudecker, S. 1989. Eye camouflage and false eyespots: Chaetodontid responses to
predators. Environ. Biol. Fishes 25:143-157.
Norman, J. R., and P. H. Greenwood 1963. A history of fishes, 2nd Ed. Benn, London,
398 pp.
Parrish, J. D., M. W. Callahan and J. E. Norris 1985. Fish trophic relationships that
structure reef communities. Proc. Int. Coral Reef Congr., 5th 4:73-78.
Parrish, J. D., J. E. Norris, M. W. Callahan, J. K. Callahan, E. J. Magarifuji and R. E.
Schroeder 1986. Piscivory in a coral reef fish community. In "Contemporary Studies on
Fish Feeding" (C. A. Simenstad and G. M. Cailliet, eds.), pp. 285-298. Junk, Dordrecht,
The Netherlands.
Partridge, B. L. 1982. The structure and function of fish schools. Sci. Am. 246:90-99.
Pietsch, T. W., and D. B. Grobecker 1978. The compleat angler: Aggressive mimicry in
an antennariid anglerfish. Science 201:369-370.
Pitcher, T. J. 1986. Functions of shoaling behaviour in teleosts. In "The Behavior of
Teleost Fishes" (T. J. Pitcher, ed.), pp. 294-337. Johns Hopkins Univ. Press, Baltimore,
Maryland.
Polovina, J. J. 1984. Model of a coral reef ecosystem. I. The ECOPATH model and its
application to French Frigate Shoals. Coral Reefs 3:1-11.
Potts, G. W. 1981. Behavioural interactions between Carangidae (Pisces) and their
prey on the fore-reef slope of Aldabra, with notes on other predators. J. Zool. 195:385404.
Randall, J. E. 1961. A contribution to the biology of the convict surgeonfish of the
Hawaiian Islands, Acanthurus triostegus sandvicensis. Pac. Sci. 15:215-272.
Randall, J. E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop.
Oceanogr. 5:665-847.
Randall, J. E., and H. A. Randall 1960. Examples of mimicry and protective
resemblance in tropical marine fishes. Bull. Mar. Sci. Gulf Caribb. 10:444-480.
Reese, E. S. 1975. A comparative field study of the social behavior and related ecology
of reef fishes of the family Chaetodontidae. Z. Tierpsychol. 37:37-61.
51
Richards, W. J. 1982. Planktonic processes affecting establishment and maintenance
of reef fish stocks. The biological bases for reef fishery management. NOAA Tech.
Mem. NMFS SEFC NMFS SEFC-80, 92-102.
Richards, W. J. and K. C. Lindeman 1987. Recruitment dynamics of reef fishes:
planktonic processes, settlement and demersal ecologies, and fishery analysis. Bull.
Mar. Sci. 41:392-410.
Richardson, S. L., J. L. Laroche and M. D. Richardson 1980. Larval fish assemblages
and associations in the north-east Pacific coast along the Oregon coast, winter-spring
1972-1975. Estuar., cstl Schelf Sci. 11:671-699.
Rimmer, D. W., and W. J. Weibe 1987. Fermentative microbial digestion in herbivorous
fishes. J. Fish Biol. 31:229-236.
Robertson, D. R. 1982. Fish feces as fish food on a Pacific coral reef. Mar. Ecol. Prog.
Ser. 7:253-265.
Robertson, D. R. 1973. Field observations on the reproductive behavior of a
pomacentrid fish, Acanthochromis polyacanthus. Z. Tierpsychol., 32:319-324.
Robertson, D. R., H. P. A. Sweatman, E. A. Fletcher, and M. G. Cleland 1976.
Schooling as a mechanism for circumventing the territoriality of competitors. Ecology
57:1208-1220.
Rosen, B. R. 1988. Progress, problems and patterns in the biogeography of reef corals
and other tropical marine organisms. Helgol. Wiss. Meeresunters. 42:269-301.
Ross, S. T. 1986. Resource partitioning in fish assemblages: A review of field studies.
Copeia 1986:352-388.
Russ, G. R., and J. St. John 1988. Diets, growth rates ans secondary production of
herbivorous coral reef fishes. Proc. Int. Coral Reef Symp., 6th 2:37-43.
Sadovy, Y. 1986. The sexual pattern and social organisation of the bicolor damselfish,
Stegastes partitus (Poey) (Pisces: Pomacentridae). Unpublished Ph.D. thesis,
University of Manchester, Manchester, England.
Sale, P. F. 1970. Distribution of larval Acanthuridae off Hawaii. Copeia 1970:765-766
Sale, P. F. 1974. Mechanisms of co-existence in a guild of territorial fishes at Heron
Island. Proc. Int. Coral Reef Symp., 2nd 1:193-206
52
Sale, P. F. 1977. Maintenance of high diversity in coral reef fish communities. Am. Nat.
111:337-359.
Sale, P. F. 1978. Coexistence of coral reef fishes - A lottery for living space. Environ.
Biol. Fishes 3:85-102.
Sale, P. F. 1979. Recruitment, loss and coexistence in a guild of territorial coral reef
fishes. Oecologia 42:159-177.
Sale, P. F. 1980a. The ecology of fishes on coral reefs. Oceanogr. Mar. Biol. 18:367421.
Sale, P. F. 1980b. Assemblages of fish on patch reefs--predictable or unpredictable?
Environ. Biol. Fishes 5:243-249.
Sale, P. F. 1985. Patterns of recruitment in coral reef fishes. Proc. Int. Coral Reef
Congr., 5th 5:391-396.
Sale, P. F. 1991a (Ed.). The Ecology of Fishes on Coral Reefs. Academic Press, San
Diego, CA, 92101, 754 pp.
Sale, P. F. 1991b. Introduction. Pgs 3-15 in P. F. Sale, ed. The Ecology of Fishes on
Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Sale, P. F. 1991c. Reef fish communities: open nonequilibrial systems. Pgs 564-598 in
P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA,
92101, 754 pp.
Sale, R. F., and R. Dybdahl 1975. Determinants of community structure for coral reef
fishes in an experimental habitat. Ecology 56:1343-1355.
Sano, M., M. Shimizu and Y. Nose 1984. Food habits of teleostean reef fishes in
Okinawa Island, southern Japan. Jpn. Univ. Mus., Univ. Tokyo Bull. 25:128pp
Schaeffer, B. and D. Rosen 1961. Major adaptive levels in the evolution of the
actinopterygian feeding mechanism. Amer. Zool. 1:187-204.
Schmitt, P. D. 1986. Feeding by larvae of Hypoatherina tropicalis (Pisces: Atherinidae)
and its relation to prey availability in One Tree Lagoon, Great Barrier Reef, Australia.
Environ. Biol. Fishes 16:79-94.
Schoener, T. W. 1983. Simple models of optimal feeding-territory size: A reconciliation.
Am. Nat. 121:608-629.
53
Scott, F. J. and G. R. Russ 1987. Effects of grazing on species composition of the
epilithic algal community on coral reefs in the central Great Barrier Reef. Mar. Ecol.
Prog. Ser. 39:293-304.
Seigel, J. A., and T. A. Adamson 1983. Batesian mimicry between a cardinalfish
(Apogonidae) and a venomous scorpionfish (Scorpaenidae) from the Philippine Islands.
Pac. Sci. 37:75-79.
Shallenberger, R. J., and W. D. Madden 1973. Luring behavior in the scorpionfish,
Iracundus signifer. Behaviour 47:33-47.
Shapiro, D. Y. 1979. Social behavior, group structure, and the control of sex reversal in
hermaphroditic fish. Adv. Study Behav. 10:43-102.
Shapiro, D. Y. 1980. Serial female sex changes after simultaneous removal of males
from social groups of a coral reef fish. Science 209:1136-1137.
Shapiro, D. Y. 1984. Sex reversal and sociodemographic processes in coral reef fishes.
In "Fish Reproduction: Strategies and Tactics" (G. W. Potts and R. J. Wootton, eds.),
pp. 103-118. Academic Press, Orlando, Florida.
Shapiro, D. Y. 1987. Differentiation and evolution of sex change in fishes. Bio-Science
37:490-497.
Shapiro, D. Y. 1989. Sex change as an alternative life-history style. In "Alternative LifeHistory Styles of Animals" (M. N. Bruton, ed.), pp. 177-195. Kluwer Academic,
Dordrecht, The Netherlands.
Shapiro, D. Y. 1991. Intraspecific variability in social systems of coral reef fishes. Pgs
331-355 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San
Diego, CA, 92101, 754 pp.
Shaw, E. 1978. Schooling fishes. Am. Sci. 66:166-175.
Shulman, M. J., J. C. Ogden, J. P. Ebersole, W. N. McFarland, S. L. Miller, and N. G.
Wolf 1983. Priority effects in the recruitment of juvenile coral reef fishes. Ecology
64:1508-1513.
Smith, S. V. 1978. Coral-reef area and the contribution of reefs to processes and
resources of the world's oceans. Nature (London) 273:225-226.
54
Smith, C. L. and J. C. Tyler 1972. Space resource sharing in a coral reef fish
community. Bull. Nat. Hist. Mus. Los Angeles County 14:125-170.
Starck, W. A. and W. P. Davis 1966. Night habits of fishes of Alligator Reef, Florida.
Ichthyologica 38:313-356.
Steneck, R. S. 1982. A limpet-coralline algal association: adaptations and defenses
between a selective herbivore and its prey. Ecology 63:502-522.
Steneck, R. S. 1988. Herbivory on coral reefs: a synthesis. Proc. Int. Coral Reef
Symp., 6th 1:37-49.
Suthers, I. M. and K. T. Frank 1991. Comparative persistence of marine fish larvae
from pelagic versus demersal eggs off south-western Nova Scotia, Canada. Mar. Biol.
108:175-184.
Sutton, D. C. and K. D. Clements 1988. Aerobic, heterotrophic gastrointestinal
microflora of tropical marine fishes. Proc. Int. Coral Reef Symp., 6th 3:185-190.
Sweatman, H. P. A. 1984. A field study of the predatory behaviour and feeding rate of a
piscivorous coral reef fish, the lizardfish Synodus englemani. Copeia 1984:187-193.
Talbot, F. H. 1965. A description of the coral structure of Tutia Reef (Tanganyika
Territory, East Africa), and its fish fauna. Proc. Zool. Soc. London 145:431-470.
Talbot, F. H., B. C. Russell and G. R. V. Anderson 1978. Coral reef fish communities:
Unstable, high-diversity systems? Ecol. Monogr. 48:425-440.
Thresher, R. E. 1983a. Environmental correlates of the distribution of planktivorous
fishes in the One Tree Reef lagoon. Mar. Ecol. Prog. Ser. 10:137-145.
Thresher, R. E. 1983b. Habitat effects on reproductive success in the coral reef fish,
Acanthochromis polyacanthus (Pomacentridae). Ecology 64:1184-1199.
Thresher, R. E. 1991. Geographic variability in the ecology of coral reef fishes:
evidence, evolution, and possible implications. Pgs 401-436 in P. F. Sale, ed. The
Ecology of Fishes on Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Thresher, R. E., P. L. Colin 1986. Trophic structure, diversity and abundance of fishes
of the deep reef (30-300 m) at Enewetak, Marshall Islands. Bull. Mar. Sci. 38:253-272.
Thresher, R. E., P. L. Colin and L. J. Bell 1989. Planktonic duration, distribution and
population structure of western and central Pacific damselfishes (Pomacentridae).
55
Copeia 1989:420-434.
Tricas, T. C. 1985. The economics of foraging in coral-feeding butterflyfishes of Hawaii.
Proc. Int. Coral Reef Congr., 5th 5:409-414.
Vermeij, G. J., and J. A. Veil 1978. A latitudinal pattern in bivalve shell gaping.
Malacologia 17:57-61.
Victor, B. C. 1983. Recruitment and population dynamics of a coral reef fish. Science
219:419-420.
Victor, B. C. 1986a. Duration of the planktonic larval stage of one hundred species of
Pacific and Atlantic wrasses (family Labridae). Mar. Biol. 90:317-326.
Victor, B. C. 1986b. Larval settlement and juvenile mortality in a recruitment-limited
coral reef fish population. Ecol. Monogr. 56:145-160.
Victor, B. C. 1987. Growth, dispersal, and identification of planktonic labrid and
pomacentrid reef-fish larvae in the eastern Pacific Ocean. Mar. Biol. 95:145-152.
Victor, B. C. 1991. Settlement strategies and biogeography of reef fishes. Pgs 231-260
in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press, San Diego,
CA, 92101, 754 pp.
Warner, R. R. 1975. The adaptive significance of sequential hermaphroditism in
animals. Am. Nat. 109:61-82.
Warner, R. R. 1988a. Sex change and the size-advantage model. Trends Ecol. Evol.
3:133-136.
Warner, R. R. 1988b. Sex change in fishes: Hypotheses, evidence, and objections.
Environ. Biol. Fishes 22:81-90.
Warner, R. R. 1991. The use of phenotypic plasticity in coral reef fishes as tests of
theory in evolutionary ecology. Pgs 387-398 in P. F. Sale, ed. The Ecology of Fishes on
Coral Reefs. Academic Press, San Diego, CA, 92101, 754 pp.
Warner, R. R., D. R. Robertson, and E. G. Leigh 1975. Sex change and sexual
selection. Science 190:633-638.
Watson, W. 1974. Diel changes in the vertical distributions of some common fish larvae
in southern Kaneohe Bay, Oahu, Hawaii. Unpulished M.S. thesis, University of Hawaii,
56
Honolulu, Hawaii
Williams, D. McB. 1980. Dynamics of the pomacentrid community on small patch reefs
in One Tree Lagoon (Great Barrier Reef). Bull. Mar. Sci. 30:159-170.
Williams, D. McB. 1991. Patterns and processes in the distribution of coral reef fishes.
Pgs 437-474 in P. F. Sale, ed. The Ecology of Fishes on Coral Reefs. Academic Press,
San Diego, CA, 92101, 754 pp.
Williams, D. McB. and A. I. Hatcher 1983. Structure of fish communities on outer slopes
of inshore, mid-shelf and outer shelf reefs of the Great Barrier Reef. Mar. Ecol. Prog.
Ser. 10:239-250.
Winn, H. E., and J. E. Bardach 1959. Differential food selection by moray eels and a
possible role of the mucous envelope of parrotfishes in reduction of predation. Ecology
40:296-298.
57
Figure 1. Summary of the life cycles of most coral reef fishes (modified from Hourigan
and Reese 1987).
Life Cycles of Coral Reef Fishes
Spawning (daily,
semilunar or lunar
during breeding season)
Pelagic Eggs
(100->100,000)
Demersal Eggs
(25-10,000)
Brooded Eggs
(100->100,000)
Fertilized eggs
leave the reef
Males guard
the eggs
Eggs brooded
orally or in
pouches (usually
by males) or
larvae born live
Eggs hatch in
the plankton
Eggs hatch and
larvae leave the
reef
Adults (seasonal
maturity in 1-5 yrs;
life span = 3-20 yrs)
Juveniles (settle
onto the reef)
Larvae (in
plankton for
9-100 days)
58
Eggs hatch/larvae
leave the reef