Coral Reefs (2005) 24: 95–98
DOI 10.1007/s00338-004-0451-5
R EP O RT
Ruth Motro Æ Inbal Ayalon Æ Amatzia Genin
Near-bottom depletion of zooplankton over coral reefs:
III: vertical gradient of predation pressure
Received: 2 July 2003 / Accepted: 31 July 2004 / Published online: 2 February 2005
Springer-Verlag 2005
Abstract Many diurnal planktivorous fish in coral reefs
efficiently consume zooplankton drifting in the overlying
water column. Our survey, carried out at two coral reefs in
the Red Sea, showed that most of the diurnal planktivorous fish foraged near the bottom, close to the shelters
from piscivores. The planktivorous fish were order of
magnitude more abundant near (<1.5 m) the bottom
than higher in the water column. The predation pressure
exerted by these fish was assessed by measuring the consumption of brine shrimps tethered at different heights
above the bottom on a vertical line which was pulled over
the reef. Below 1.5 m above bottom, the shrimps’ survival
probability sharply decreased toward the bottom. Higher
in the water column, survivorship was nearly 100% with
little vertical variation. Our results indicate that nearbottom depletion of zooplankton in coral reefs is likely
due to intense predation at that boundary layer. Risk of
predation by piscivorous fish apparently restricts planktivorous fish to forage near the bottom, with a distribution
pattern greatly deviating from ideal-free distribution.
Keywords Fish Æ Planktivores Æ Piscivores Æ Vertical
gradients Æ Artemia Æ Red Sea
Introduction
Predation on zooplankton by fish in coral reefs is intense
(Hamner et al. 1988). A large portion of the zooplankCommunicated by Ecological Editor Peter Sale
R. Motro Æ I. Ayalon Æ A. Genin (&)
The H. Steinitz Marine Biology Laboratory,
The Interuniversity Institute for Marine Sciences of Eilat,
P.O.B. 469, Eilat, 88103, Israel
E-mail: [email protected]
Tel.: +972-8-6360143
Fax: +972-8-6374329
R. Motro Æ A. Genin
The Department of Evolution Systematics and Ecology,
The Hebrew University of Jerusalem, Israel
ton drifting over the reef during the day can be rapidly
devoured by planktivorous fish (Glynn 1973; Johannes
and Gerber 1974; Hamner et al. 1988; Genin et al. 1995).
Such strong diurnal zooplanktivory is one possible
mechanism accounting for the migratory behavior of
demersal zooplankton, the group of zooplankton that
resides near the bottom during the day and rises into the
water column at night (Alldredge and King 1977). Visual predation may also account for the dominance of
small zooplankters, which are less prone to predation,
above coral reefs during the day (Ohlhorst 1982). In
addition, planktivorous fish can affect local recruitment
of benthic organisms by their feeding on planktonic
larvae (Gaines and Roughgarden 1987; Olson and
McPherson 1987).
In turn, the abundance of planktivorous fish in many
coral reefs is determined by predatory fish (e.g. Hobson
1975; Prejs 1987; Holbrook and Schmitt 1988; Caley
1993; Beets 1997; Steele 1999; Connell 2002). Piscivorous fish also affect the distribution of zooplanktivorous
fish, which seek shelter in, and forage in close proximity
to branching corals and perforated topography (Clarke
1992; Beukers and Jones 1998; Bullard and Hay 2002).
The confinement of diurnal planktivorous fish to the
proximity of the bottom should intensify zooplanktivory
near the bottom. This hypothesis is indirectly supported
by recent studies (Holzman et al. 2004; Yahel et al.
2004), showing near-bottom depletion of zooplankton.
In this study, we measured the vertical gradient in
zooplanktivory above coral reefs and tested for correspondence between the observed gradient and the distribution of planktivorous fish.
Methods
The study was carried out at two coral reefs and a sandy
site near Eilat, the Gulf of Aqaba (Israel): (1) the coral
reef off the Steinitz Marine Biology Laboratory (MBL,
2930¢N, 3455¢E), (2) the coral reef between the two
piers of the oil terminal (OT, 2931¢N, 3456¢E), and (3)
96
the sandy bottom at the Dekel Beach (2932¢N,
3457¢E). The fringing coral reefs in the region have
approximately 60% cover of rocky substratum; about
half of it is live corals (Israel National Monitoring
Program, unpublished report). Many planktivorous fish
are found close to the bottom in those reefs, with a
dominance of the genera Dascyllus, Pomacentrus and
Pseudanthias. The overlaying waters are inhabited by
schools of planktivores such as Abudefduf saxatilis and
Caesio lunaris (Rilov and Benayahu 2000). The sandy
site has 100% sand cover and planktivores are very rare.
The study consisted of two parts, a fish survey and in
situ predation experiments, all carried out by scuba divers between September 2002 and April 2003.
Fish surveys
Planktivorous fish were counted by two divers along
seven (at MBL) or eight (at OT) randomly positioned
25 m·1 m belt transects at 6–8 m bottom depth. Each
transect was marked beforehand by stretching two
measuring tapes 1 m apart. The water column above the
transect was divided into two zones, the zone from the
bottom to 1.5 m above bottom (mab) and the zone
above it, up to the surface. The two divers swam together one above the other at a speed of ca. 10 cm s 1,
with one diver at 1 mab and the other directly above
the first one. The lower diver counted the fish at the
lower layer while at the same time the other diver
counted the fish at the upper layer. The 1.5 mab
demarcation height between the two layers was chosen
based on earlier observations (Yahel et al. 2004; Holzman et al. 2004) indicating that the benthic layer depleted of zooplankton at the MBL site extended up to
that height. Both divers kept their positions in the water
column by using accurate depth gauges (±0.1 m). Our
counts could have missed small cryptic fish hiding in
crevices or in the substrate. A few fish (<1%) found
near the 1.5 mab demarcation height could have been
skipped due to our conservative approach to avoid
counting of the same fish by both divers.
Predation experiments
The experiment measured the predation on zooplankton
tethered to a taut line at different heights above bottom,
Fig. 1 The ‘‘vertical Artemia
line’’ carrying 12 tethered
shrimps being pulled
downstream by a drifting diver
(right) along the ‘‘rail line’’ on
the bottom. To minimize
disturbance to the foraging fish,
the diver was always >25 m
downstream of the Artemia line
pulled along 21, 12, and 15 different tracks at MBL, OT,
and the Dekel Beach, respectively. The tracks, each 20 m
long, were at 6 m depth. Adult brine shrimp (Artemia
salina) without ovisac, with body length 10–15 mm were
served as live prey. Each shrimp was tied from the
abdomen to a 5 cm long nylon thread (300 lm diameter), without restraining the movement of the phyllopods
on the thorax. Adult shrimps were used since we were
unable to tether smaller shrimps with their phyllopods
free to move. The shrimps were tied by their thread to a
vertical, 6 m long transparent fishing line tautly rising
into the water column by a buoy attached to its upper
end and connected at its lower end to a line on the reef
through a small ring (Fig. 1). A total of 12 shrimps were
tied 0.5 m apart from 0.5 mab to the surface (hereafter
‘‘vertical Artemia line’’). Each track was placed by
haphazardly selecting a point from which a thin 20 mlong line was stretched and laid on the bottom along the
6 m depth contour. This line served as a ‘‘rail’’, guiding
the motion of the vertical Artemia line, pulled by a distant diver using a horizontal extension string tied to the
bottom ring (Fig. 1). The array was pulled in the
direction and at the approximate speed of the ambient
water current. At the end of each ‘‘pull’’, lasting 3–5 min
(flow speed dependent) the divers counted the remaining
prey.
Tests done prior to the experiment showed that
dominant planktivorous fish at our study site, including
Pomacentrus trichourus, Dascyllus marginatus, Dascyllus
aruanus, Amphiprion bicinctus, and Neopomacentrus
miryae (Randall 1967), readily removed and ate the
tethered shrimps.
In order to test for possible disappearance of tethered
Artemia for reasons other than predation (e.g., escape,
being torn off by reef objects), we carried out 20 ‘‘control runs’’. Five of those runs were carried out at MBL
reef during the night, when diurnal planktivorous fish
are inactive and nocturnal fish are rare. The other 15
control runs were carried out during the day at Dekel
Beach, a sandy bottom site at which no planktivorous
fish were observed during our underwater sessions.
Each run was regarded as a single binomial test, and
the total of all runs for each site was pooled yielding the
frequency of survival at each height. Confidence intervals for these frequencies were calculated using the
Wilson score method with no continuity correction
(Newcombe 1998). The number of runs at each site
(21 at MBL, 12 at OT) exceeded the sample size re-
97
quired to detect a true difference between the frequencies
according to Casagrande, Pike and Smith (1978) (pp
766–767 in Sokal and Rolf 1981).
Results
The density of zooplanktivorous fish was significantly
greater at <1.5 mab than higher in the water column at
both MBL and OT. The guilds of zooplanktivorous fish
at the two sites were similar, consisting mostly of the
following species: Amblyglyphidodon leucogaster, Chromis viridis, Dascyllus aruanus, Dascyllus marginatus,
Dascyllus trimaculatus, and Pomacentrus trichourus.
Only D. trimaculatus regularly foraged above 1.5 mab.
The density of fish foraging <1.5 mab was approx.
30 and 20 times greater than higher in the water column
at MBL and OT, respectively (P<0.0001 at each site;
one tailed t-test) (Fig. 2). The vertical pattern in predation pressure (Fig. 3) closely corresponded to the fish
distribution, with a sharp decrease in prey survival near
the bottom. The probability for a tethered shrimp to
survive a 20 m ‘‘pull’’ closest to the bottom (0.5 mab)
was 0.38 or 0.42 at MBL and OT, respectively. The
overall survival probability at <1.5 mab was ca. 1.6
times lower than in the layer above (Wilcoxon matchedpairs signed-ranks test, P<0.01) at each of the two coral
reefs. No shrimp was lost (100% survival) at the control
runs, neither over the sandy site nor at night.
caped the tether, indicated that the loss of shrimps at the
reef could be attributed to predation.
Our observations corroborate the assertion that the
vertical zooplankton gradients above coral reefs during
the day (Yahel et al. 2004; Holzman et al. 2004) were due
to a corresponding gradient in predation pressure. Vertebrate predation can be sufficiently strong to influence
the distribution patterns of zooplankton (e.g. in marine
bays—Kimmerer and McKinnon 1989). The role of
actual predation in determining the gradient is in
agreement with the pattern of the stronger gradient for
the relatively stronger swimming taxa (Holzman et al.
2004), as stronger swimming increases detectability by
visual zooplanktivorous fish and enhances encounter
rates (Curio 1976; McFarland and Levin 2002). Coralreef planktivores are well adapted to capture evading
prey (Coughlin and Strickler 1990).
Our experiment was designed to yield a relative
measure of predation pressure at different heights above
bottom. By no means should the predation values we
measured (Fig. 3) be applied to true predation pressure
on native zooplankton in the reef. First, the brine
shrimps were much larger than the normal prey found in
the reef during the day (A. Genin, unpublished data).
Secondly, unlike most marine taxa, Artemia salina does
not exhibit an escape response from predators (Trager
et al. 1994); moreover, the shrimps were tethered to a
line. However, our experiment provides an unambiguous
relative proxy of predation pressure at different heights
above bottom. Other studies show that plankton tethering is a good method for evaluating spatial differences
Discussion
Our results revealed the occurrence of a very strong
gradient of increasing predation pressure below
1.5 mab, the apparent product of a much higher density of zooplanktivorous fish in that layer. The control
experiments, in which no single shrimp fell off or es-
Fig. 2 The average abundance (±SD) of zooplanktivorous fish at
the two layers (below and above 1.5 m above bottom) at the MBL
and OT coral reefs
Fig. 3 The probability of survival for an Artemia pulled for 20 m
along the coral reef at MBL (a) and OT (b) as a function of height
above bottom. Error bars are 95% confidence intervals. (N=21 at
MBL and 12 at OT)
98
in predation pressure (Acosta and Butler 1999; Bullard
and Hay 2002)
The distribution of planktivorous fish does not match
the pattern expected under the predictions of ideal free
distribution (IFD) (Ricklefs 2000). According to our fish
transects, some 30 times more fish are found in the layer
where the prey density is half that of the layer nearby
(Yahel et al. 2004). This strong deviation from IFD can
be clearly attributed to predation risk by piscivorous
fish. When offered shelter higher up in the water column,
fish prefer using that shelter and forage at the upper
water column, where they grow faster and have higher
fecundity than individuals residing at the near bottom
layer (Clarke 1992). Through their effect on the foraging
behavior of planktivorous fish, piscivores may indirectly
shape the vertical distribution of zooplankton at the
coral reef.
Acknowledgements We would like to thank A. Maoz, D. Sadowitz,
I. Atad, J. Belmaker, O. Steinitz, R. Ben-David Zaslo, R. Kent and
S. Einbinder for helping with the field work. We thank KATZA oil
company for access to their coral reef. We are grateful to the Interuniversity Institute for Marine Sciences of Eilat for logistic
support and to Dr. M. Shpigel for providing the brine shrimps.
Special thanks to Michal and Uzi Motro for their help and support
all along the way. This research was supported by the Israel Science
Foundation, funded by the Israel Academy of Science and
Humanities.
References
Acosta CA, Butler MJ IV (1999) Adaptive strategies that reduce
predation on Carribean spiny lobster postlarvae during onshore
transport. Limnol Oceanogr 44:494–501
Alldredge AL, King JM (1977) Distribution, abundance and substrate preference of demersal reef zooplankton at Lizard Island
Lagoon, Great Barrier Reef. Mar Biol 41:317–333
Beets J (1997) Effects of predatory fish on the recruitment and
abundance of Carribean coral reef fishes. Mar Ecol Prog Ser
148:11–21
Beukers JS, Jones GP (1998) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia
114:50–59
Bullard SG, Hay ME (2002) Plankton tethering to assess spatial
patterns of predation risk over a coral reef and sea grass bed.
Mar Ecol Prog Ser 225:17–28
Caley MJ (1993) Predation, recruitment and the dynamics of
communities of coral-reef fishes. Mar Biol 117:33–43
Clarke RD (1992) Effects of microhabitat and metabolic rate on
food intake, growth and fecundity of two competing coral reef
fishes. Coral Reefs 11:199–205
Connell SD (2002) Effects of a predator and prey on a foraging reef
fish: implications for understanding density-dependent growth.
J Fish Biol 60:1551–1561
Coughlin DJ, Strickler JR (1990) Zooplankton capture by a coral
reef fish an adaptive response to evasive prey. Environ Biol Fish
29:35–42
Curio E (1976) The ethology of predation. Springer, Berlin Heidelberg New York
Gaines S, Roughgarden J (1987) Fish in offshore kelp forests affect
recruitment to intertidal barnacle populations. Science 235:479–
481
Genin A, Gal G, Haury L (1995) Copepod carcasses in the ocean:
II. Near coral reefs. Mar Ecol Prog Ser 123:65–71
Glynn PW (1973) Ecology of a Caribbean coral reef. The Porites
reef-flat biotope: Part II. Plankton community with evidence for
depletion. Mar Biol 22:1–21
Hamner WM, Jones MS, Carleton JH, Hauri IR, Williams DMcB
(1988) Zooplankton, planktivorous fish, and water currents on
a windward reef face: Great Barrier Reef, Australia. Bull Mar
Sci 42:459–479
Hobson ES (1975) Feeding patterns among tropical reef fishes. Am
Sci 63:382–394
Holbrook SJ, Schmitt RJ (1988) Effects of predation risk on foraging behavior: mechanisms altering patch choice. J Exp Mar
Biol Ecol 121:151—163
Holzman R, Reidenbach MA, Monismith SG, Koseff JR, Genin A
(2004) Near-bottom depletion of zooplankton over a coral reef:
II. Relationships with zooplankton swimming ability. Coral
Reefs (this issue)
Johannes RE, Gerber R (1974) Import and export of net plankton
by an Eniwetok coral reef community. In: Proceedings of the
2nd international coral reef symposium, vol 1. Great Barrier
Reef Committee, Brisbane, pp 97–104
Kimmerer WJ, McKinnon AD (1989) Zooplankton in a marine
bay III. Evidence for influence of vertebrate predation on distributions of two common copepods. Mar Ecol Prog Ser 53:21–
35
McFarland W, Levin SA (2002) Modelling the effects of current on
prey acquisition in planktivorous fishes. Mar Fresh Behav
Physiol 35:69–85
Newcombe RG (1998) Two-sided confidence intervals for the single
proportion: comparison of seven methods. Stat Med 17:857–
872
Ohlhorst SL (1982) Diel Migration patterns of demersal reef zooplankton. J Exp Mar Biol Ecol 60:1–15
Olson RR, McPherson R (1987) Potential vs. realized larval dispersal: fish predation on larvae of the ascidian Lissoclinum
patella (Gottschaldt). J Exp Mar Biol Ecol 110:245–256
Prejs A (1987) Risk of predation and feeding rate in tropical
freshwater fishes: field evidence. Oecologia 72:259–262
Randall JE (1967) Food habits of reef fishes of the West Indies.
Stud Trop Oceanogr 5:665–847
Ricklefs RE, Miller GL (2000) Ecology. WH Freeman and Co,
New York, pp 655–656
Rilov G, Benayahu Y (2000) Fish assemblages on natural vs artificial reefs: the rehabilitation prespective. Mar Biol 136:931–942
Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman and Co, San
Francisco, pp 766–767
Steele MA (1999) Effects of shelter and predators on reef fishes. J
Exp Mar Biol Ecol 233:65–79
Trager G, Achituv Y, Genin A (1994) Effects of prey escape ability,
flow speed, and predator feeding mode on zooplankton capture
by barnacles. Mar Biol 120:251—259
Yahel R, Yahel G, Genin A (2004) Near-bottom depletion of
zooplankton over coral reefs: I Diurnal dynamics and size
distribution. Coral Reefs