Predator-Induced Demographic Shifts in Coral Reef Fish
Benjamin I. Ruttenberg1,2, Scott L. Hamilton1,3, Sheila M. Walsh4¤, Mary K. Donovan1,5, Alan
Friedlander5, Edward DeMartini6, Enric Sala7,8, Stuart A. Sandin4*
1Marine Science Institute, University of California Santa Barbara, Santa Barbara, California, United States of America, 2National Marine Fisheries Service, Southeast
Fisheries Science Center, Miami, Florida, United States of America, 3Moss Landing Marine Laboratories, Moss Landing, California, United States of America, 4Scripps
Institution of Oceanography, La Jolla, California, United States of America, 5United States Geological Survey, Hawaii Cooperative Fishery Research Unit, University of
Hawaii, Honolulu, Hawaii, United States of America, 6National Marine Fisheries Service, Pacific Islands Fisheries Science Center, Aiea, Hawaii, United States of America,
7Centre d’Estudis Avanc ¸ats de Blanes, Consejo Superior de Investigaciones Cientı ´ficas, Blanes, Spain, 8National Geographic Society, Washington, D.C., United States of
In recent years, it has become apparent that human impacts have altered community structure in coastal and marine
ecosystems worldwide. Of these, fishing is one of the most pervasive, and a growing body of work suggests that fishing can
have strong effects on the ecology of target species, especially top predators. However, the effects of removing top
predators on lower trophic groups of prey fishes are less clear, particularly in highly diverse and trophically complex coral
reef ecosystems. We examined patterns of abundance, size structure, and age-based demography through surveys and
collection-based studies of five fish species from a variety of trophic levels at Kiritimati and Palmyra, two nearby atolls in the
Northern Line Islands. These islands have similar biogeography and oceanography, and yet Kiritimati has ,10,000 people
with extensive local fishing while Palmyra is a US National Wildlife Refuge with no permanent human population, no fishing,
and an intact predator fauna. Surveys indicated that top predators were relatively larger and more abundant at unfished
Palmyra, while prey functional groups were relatively smaller but showed no clear trends in abundance as would be
expected from classic trophic cascades. Through detailed analyses of focal species, we found that size and longevity of a top
predator were lower at fished Kiritimati than at unfished Palmyra. Demographic patterns also shifted dramatically for 4 of 5
fish species in lower trophic groups, opposite in direction to the top predator, including decreases in average size and
longevity at Palmyra relative to Kiritimati. Overall, these results suggest that fishing may alter community structure in
complex and non-intuitive ways, and that indirect demographic effects should be considered more broadly in ecosystem-
Citation: Ruttenberg BI, Hamilton SL, Walsh SM, Donovan MK, Friedlander A, et al. (2011) Predator-Induced Demographic Shifts in Coral Reef Fish
Assemblages. PLoS ONE 6(6): e21062. doi:10.1371/journal.pone.0021062
Editor: Peter Roopnarine, California Academy of Sciences, United States of America
Received October 23, 2010; Accepted May 19, 2011; Published June 16, 2011
Copyright: ? 2011 Ruttenberg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by E. Scripps and other anonymous donors contributing money to the Scripps Institution of Oceanography. The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: email@example.com
¤ Current address: The Nature Conservancy, Arlington, Virginia, United States of America
Understanding the factors that lead to variation in coral reef fish
populations and community structure is critically important to
improving conservation and fisheries management. Over the past
decades, it has become increasingly clear that human activities have
altered ecological structure in many coastal systems through
processes such as fishing, pollution, and climate change [1–3].
Fishing has a variety of direct effects on most coral reef ecosystems,
throughout the tropics. Changes in individual sizes of target species
and subsequent alterations of community structure resulting from
fishing have been well-documented in many systems worldwide
[1,2,4,5]. However, these effects are likely not restricted to changes
in abundance or size, but may include changes in demography and
life histories that are more difficult to detect, and yet may still
strongly influence the ecology of these systems.
Few studies have examined changes in demography and life
history of individual species as a result of fishing, and nearly all of
these have examined fishery target species [6–10]. Findings
commonly show that fishing directly reduces longevity, mean
and maximum size, and the size and age at maturation and sex
change of targeted fishery species. A number of studies have
examined spatial variability in demography and life-history of non-
target reef fish, but these studies have generally focused on the
influence of large-scale geography or environmental factors such
as temperature [11–16]. Indirect effects of fishing on demographic
patterns of non-target species have been generally neglected (but
see [17,18]), in part because detecting such changes can be
difficult, especially in systems that have experienced significant
changes in community structure as a result of overexploitation.
Indirect effects can result from cascading effects of removal (or
restoration) of top trophic groups. In most coral reef systems, top
predators (e.g., sharks and larger groupers, snappers, and jacks) are
PLoS ONE | www.plosone.org1June 2011 | Volume 6 | Issue 6 | e21062
often the most sought-after species in a fishery and therefore subject
to the strongest fishing pressure. General ecological theory predicts
that reductions in abundances of top predators should lead to
reductions in rates of predation on lower trophic groups and ‘prey
release,’ i.e. the increase in prey populations following reductions of
predator density [4,19], which may result in a classic trophic
less prevalent in marine environments. When present, trophic
cascades often involve sea urchins or other echinoderms and
specialist predators, and are generally more common in temperate
than tropical regions [20–22]. The complexity of tropical marine
food webs appears to reduce the prevalence of prominent trophic
cascades, and there are few if any documented trophic cascades in
coral reef fish assemblages ( but see [23,24]). Even though
numerical trophic cascades are rare in marine systems, indirect
effects on demography or life histories of prey species may occur,
and such indirect effects may have strong impacts throughout the
community. For example, changes in species composition, size or
longevity of grazers can strongly influence grazing rates, which can
in turn influence abundance of some groups of algae that compete
with corals for space on the reef [25–27].
Because trophic connections among coral reef fish species are
diffuse within complex food webs, we may not expect simple linear
trophic cascades, in which decreases in top predators lead to
increases in secondary consumers, resulting in decreases in
primary consumers, and so forth. Descriptions of reef fish
assemblages from the Caribbean , the central Pacific ,
and the Indian Ocean  show no clear evidence of guild-level
release and commensurate trophic cascades within fish assem-
blages, even among areas that differ in abundance of top
predators. Instead, top predators on coral reefs tend to be
generalists and are likely feeding on a variety of fishes and
invertebrates from several lower trophic groups.
Although there is little evidence that fishing results in prey
release or trophic cascades on coral reefs, demographic traits of
prey may still respond to removal of top predators. For example,
when predatory fish are removed by fishing, demographic traits
such as size and longevity may increase for non-targeted species in
lower trophic levels because of reductions of predation intensity or
predation risk. Therefore, we predict that where top predators are
removed by fishing, prey fishes will live longer and attain larger
sizes. If changes in predation and associated demographic shifts
are extreme or persistent enough, we expect that changes in
growth and life history may also occur for these species, analogous
to those observed in directly exploited species .
In most coral reef locations, fish assemblages have been
significantly altered for decades or even centuries due to
anthropogenic influences, such as fishing, reductions in water
quality, and loss of live coral and other associated habitats (e.g.
seagrasses, mangroves). In many locations, densities of top
predators, such as sharks and large snappers and groupers, have
been so reduced that they no longer serve whatever ecological role
they may have had in the past [2,32–36]. However, the ideal
system to examine predator-induced demographic shifts should
include some areas that are free or nearly free of human and/or
fishing impacts and other areas that are subject to fishing pressure.
The Northern Line Islands in the central Pacific possesses many of
these ideal characteristics. Recent work in this archipelago has
found significant changes in population and community structure
along a gradient of human disturbance, including changes in fish
assemblages , benthic communities , microbial communi-
ties , and parasite communities . Most importantly for
examining indirect demographic shifts in coral reef fishes, top
predator abundance in unfished locations is nearly as high as any
other documented coral reef system, and is much lower in the
fished areas [18,29,39]. We used two of the Northern Line Islands
(unfished Palmyra and fished Kiritimati) to examine predator-
induced demographic shifts in five different species of coral reef
fishes from a variety of trophic levels. We found that top predators
were larger and longer lived at unfished Palmyra relative to fished
Kiritimati, but that species in lower trophic groups were generally
smaller and experienced higher rates of mortality at Palmyra
relative to Kiritimati. These results suggest that even the absence
of clear numerical trophic cascades, demographic rates of non-
target species may be influenced by the removal of top predators.
The Northern Line Islands is a remote archipelago that spans
650 km between 1.75u–6.5uN and 157u–162.5uW in the central
Pacific, located approximately 1500 km south of the Hawaiian
Archipelago. Previous work in this archipelago has found that a
number of putative metrics of ecosystem health, such as total fish
biomass, predatory fish biomass, and cover of reef-builders (i.e.
stony corals and crustose coralline algae) correlate negatively with
human population size; conversely, putative metrics of ecosystem
degradation, such as concentration of microbes, potential
pathogens, and prevalence of coral disease correlate positively
with human population [29,37]. In this study, we compare fish
assemblages between two of these islands with very different levels
of human impacts, Palmyra Atoll and Kiritimati Atoll (Fig. 1).
Palmyra has been a U.S. National Wildlife Refuge since 2001;
fishing and non-scientific extraction are prohibited and were
limited for decades prior, and the atoll houses only a small
research station. Kiritimati Atoll, part of the Republic of Kiribati,
has a population of ,10,000 people, with most living on the
northwestern part of the island where artisanal fishing and
aquarium fish collecting are concentrated. The remote nature of
the Line Islands makes conducting fieldwork difficult and
expensive; we chose to sample Palmyra and Kiritimati because
they differ greatly in human impacts and because they are the only
two islands in the archipelago with managed runways, enabling
reliable land-based field logistics.
Underwater visual surveys were used to quantify densities and
size distributions for all non-cryptic species (see [18,29] for
methodological details). A pair of divers counted all fish within
adjacent 25-m long transects, with the width of the transect scaled
depending on the size of the fish (for each diver, a 4-m wide ‘swim-
out’ counting all fish $20 cm total length [TL], and a 2-m wide
‘swim-back’ counting fish ,20 cm TL). At each station, divers
surveyed three transects, with the team surveying 600 m2for
larger fish and 300 m2for smaller fish. Divers surveyed 26 stations
at Palmyra and 25 stations at Kiritimati along the forereef at 10 m
We selected among the most abundant species in each major
trophic group for collections and detailed investigation of
demography and life history. Lutjanus bohar, the two-spot red
snapper, is a common top predator that feeds on fish and
invertebrates and is preyed upon only by sharks. Paracirrhites arcatus,
the arc-eye hawkfish, is a mid-level predator usually associated
with small branching corals, which feeds primarily on benthic
crustaceans. Chromis margaritifer, the bicolor chromis, is an
abundant, shoaling planktivore. Plectroglyphidodon dickii, the black-
bar devil, is an omnivore that establishes territories of algal turf but
also feeds on small invertebrates. Acanthurus nigricans, the white-
cheek surgeonfish, is a mobile herbivore that feeds primarily on
turf algae. We used a variety of methods to collect individual fish,
including netting, spearing, clove oil, hook and line, and assistance
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org2 June 2011 | Volume 6 | Issue 6 | e21062
from local fishers on Kiritimati, attempting in all cases to obtain a
representative sample of the size range observed in the field. All
collections were made on the forereefs of the two islands, between
5 and 20 m depth. Because Palmyra is a National Wildlife Refuge,
we were limited to collecting no more than 50 individuals of each
species at that island and sample sizes were similar at Kiritimati.
See Table 1 for a summary of collections.
Upon collection, samples were immediately transported to the
lab for processing. Each specimen was weighed, measured, and
sexed by gross examination of the gonads. The sagittal otoliths
were removed, cleaned, and stored dry. Otolith preparation
generally followed Robertson et al. . Sagittal thin sections were
examined under a compound microscope at 40–1006magnifica-
tion using transmitted light. Annuli were interpreted using
standard techniques  and each otolith was examined by at
least two readers. When age estimates differed by more than 10%,
a third reader examined the sample. When annuli were not
interpretable after examination by three readers, the second sagitta
was processed, and individuals for which both otoliths were
unreadable were excluded from the analysis.
We calculated station-specific estimates of density and mean
length for each species from survey data. To test for differences
between islands, we compared these values using two-sample
t-tests of station-specific estimates (n=26 for Palmyra, n=25 for
Kiritimati), using log-transformations when necessary to reduce
variance heterogeneity. To examine changes in size structure across
all species in the assemblage, we calculated summary statistics of fish
length estimates relative to species-specific maximum lengths. For
each fish counted, we converted length to a proportion (between 0
and 1) reflecting the size of the individual relative to the largest
individual recorded in the region (calculated from a database of reef
fish length estimates from the Northern Line Islands ). For
example, an individual fish of length 30 cm for which the largest
individual of that species was 40 cm would be assigned a value of
Figure 1. Map of the Line Islands, including Palmyra and Kiritimati.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org3 June 2011 | Volume 6 | Issue 6 | e21062
0.75. We computed station-specific mean estimates of length in
units of standardized length (fraction of species-specific maximum
length), and compared these estimates across islands for different
trophic groups as described above.
To compare longevity across islands, we calculated the mean of
the top quartile of age in years (Tmax, after ) for each species
on each island, which allows us to compare across collections with
small or variable sample sizes. We described growth using island-
specific von Bertalanffy growth functions (VBGF): Lt=Linf
(12exp([2k(t2t0)]), where Lt is length at age t, Linf is mean
asymptotic length, k describes the rate at which the asymptotic
length is attained, t is the age in years, and t0is a theoretical age at
which length is 0. Estimates of t0are sensitive to small sizes and
ages; because our collections had few small/young individuals, we
constrained t0to 0 in all cases . We focus on the parameters
Linf and k, which provide population-level estimates for mean
maximum size (e.g. asymptotic length) and the rate at which that
length is reached (a proxy for growth rate). However, since recent
work has suggested modifications to the VBGF to enhance
interpretability of the parameters Linf and k , we include
calculations for a re-parameterized VBGF (Text S1, Table S1). To
test whether growth curves differed significantly among atolls for
each species, we compared AIC values for VBGF models that
pooled samples between islands and VBGF models that fit growth
curves separately for each island. For each species, statistical
significance was determined in cases where the difference in AIC
values (DAIC) between the 2-parameter and 4-parameter models
was $2 . We calculated 95% confidence regions around
estimates of Linfand k following Kimura . All analyses were
conducted using R v.2.10 .
Abundance estimates differed between islands for all 5 species
(p,0.05 in all cases; Table 1). Density of L. bohar, a top predator,
was lower at fished Kiritimati relative to protected Palmyra. The
remaining four prey species showed no consistent trend in
abundance, with two species more abundant at Kiritimati (C.
margaritifer and P. dickii) and two species more abundant at Palmyra
(P. arcatus and A. nigricans), suggesting that numerical trophic
cascades are not present in this system. However, despite the lack of
evidence for classic trophic cascades, mean size as estimated by
visual surveys differed significantly between islands for 4 of the 5
species (Fig. 2a). The mean size of L. bohar was larger at Palmyra
relative to Kiritimati (p,0.05). In contrast, three of the four prey
species, P. arcatus, C. margaritifer, and A. nigricans, were larger at
Kiritimati (p,0.05; Fig. 2a). A similar relative pattern of size held
across the entire fish assemblage. The mean size of top predators
(estimated as a proportion relative to species-specific maximum
sizes) was significantly larger at Palmyra. In contrast, the mean
relative size of all fish was significantly larger at Kiritimati (Fig. 2b).
Mean size of fish within two of the three trophic groups of prey,
benthicinvertivores and zooplanktivores,were significantly largerat
Kiritimati (p,0.05), while herbivores did not differ in size between
islands (Fig. 2b). Longevity, calculated as the mean of the top
quartile of the collections , differed greatly between islands for 4
of the 5 species. Longevity for the predator L. bohar was significantly
greater at Palmyra than Kiritimati, while longevity for three of the
four prey species, P. arcatus, P. dickii, and A. nigricans, was significantly
greater at Kiritimati versus Palmyra (p,0.001 in all cases; Fig. 2c).
Longevity did not differ for C. margaritifer between islands.
We estimated the parameters Linfand k from the VBGF for the
five species from each island (Table 1). For each species, the
parameters of the VBGF differed significantly between islands
(DAIC$2.0 for each species when comparing a 2-parameter model
[i.e.,pooling data between islands foreachspecies] toa 4-parameter
model [independent parameters fit for each island]). Inspection of
95% confidence intervals for the best-fit parameters of the species-
and island-specific VBGFs illustrates the qualitative direction of
difference for each species (Fig. 3). The estimate of Linf was
significantly greater (and k was significantly smaller) at Palmyra
relative to Kiritimati for the top predator, L. bohar, indicating that
this species attained larger maximum sizes and reached those sizes
at a slower rate at Palmyra compared to Kiritimati. A similar, but
weaker, pattern existed for C. margaritifer. In contrast, Linf was
significantly greater at Kiritimati relative to Palmyra for P. arcatus
and A. nigricans, and k was significantly greater at Palmyra for P.
arcatus (Fig. 3, Table 1). The estimate of k trended toward smaller
values at Kiritimati relative to Palmyra for P. dickii (Fig. 3).
the role played by top predator fishes in reef fish assemblages.
Table 1. Samples sizes, mean numerical densities (abundance), parameter estimates for Linfand k, and DAIC values for each
species at each island.
SpeciesIslandSample Size (N)Mean Density (# 100 m22)Linf(cm)k (year21)
L. boharKiritimati65 1.5 (0.3)30.4 (1.03)0.3 (0.03)
Palmyra 204.1 (0.5) 49.9 (1.70)0.1 (0.01)
P. arcatus Kiritimati572.6 (0.4)8.3 (0.20)0.4 (0.03)
Palmyra487.8 (0.9)7.3 (0.23)0.7 (0.08)
C. margaritifer Kiritimati 63153.3 (25.6) 5.1 (0.12)0.4 (0.03)
Palmyra4551.4 (7.9)5.8 (0.14)0.3 (0.02)
P. dickiiKiritimati54 7.0 (1.5)5.6 (0.12)0.5 (0.05)
Palmyra402.7 (0.5)5.5 (0.11)0.5 (0.04)
A. nigricans Kiritimati 671.9 (0.3)15.3 (0.25)0.7 (0.09)
Palmyra427.0 (0.8)14.3 (0.34)0.5 (0.07)
Values in parentheses are standard errors, and DAIC is the difference between AIC values for each species for separate VBGF models fit for each island compared to
single model fit for each species.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org4June 2011 | Volume 6 | Issue 6 | e21062
Figure 2. Size, maximum length and longevity between islands. A) Sizes of the five study species at each island from survey data (mean
length 61 SE). B) Proportion of maximum sizes for each trophic group and all fish combined from the full species assemblage for each island, based
on maximum sizes for each species from survey data (mean proportion of maximum length 61 SE). C) Longevity for the 5 study species (Tmax, mean
of top quartile, 695% CI). Data for Palmyra are in black, data for Kiritimati are in gray.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org5 June 2011 | Volume 6 | Issue 6 | e21062
Between fished Kiritimati (population of ,10,000 with intensive
subsistence fishing ) and unfished Palmyra (protected as a US
National Wildlife Refuge since 2001), there is a .8-fold difference
in biomass of top predators (and a .3-fold difference if reef sharks
are excluded [18,29]). In contrast to predators, there is no consistent
pattern in the biomass or abundance of lower trophic levels ,
with no evidence of trophic cascades or even of simple prey release
at the guild-level. Focusing on five of the most abundant species in
the assemblage, we find a similar lack of clear density changes that
are generally associated with tight trophic links. While the density of
the top predator, L. bohar, was reduced at Kiritimati, the densities of
the four prey species showed inconsistent patterns (i.e. two of the
prey species had higher densities at Palmyra, and two had higher
densities at Kiritimati; Table 1).
Even though we found no evidence for prey release and classic
trophic cascades, changes in predator assemblages may still result
in demographic changes on lower trophic levels that are more
difficult to detect. We predicted that size structure would be shifted
toward smaller sizes and longevity would be lower in prey fishes in
locations where predator assemblages are intact. Furthermore,
because of the trophic complexity of coral reef fish assemblages,
we predicted that these demographic shifts would occur in the
same direction for all lower trophic levels, and not alternate
among trophic levels as in other systems as predicted by classical
ecological theory [45,46].
In general, differences in demographic parameters met our
predictions for most species and trophic groups, particularly for
mean size and longevity (Tmax, Fig. 2). Mean size differed as
predicted for 3 out of 4 trophic groups and for 4 of 5 species, and
longevity differed as predicted for 4 of 5 species (i.e., increases for
the top predator and decreases for all lower trophic levels at
unfished Palmyra). These results suggest that changes in predator
Figure 3. Size-at-age relationships for the 5 study species by island, with lines of best fit for VBGF parameters. Inset plots for each
species show 95% confidence ellipses for the parameters k and Linf. Shading for histogram bars as in Fig. 2.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org6June 2011 | Volume 6 | Issue 6 | e21062
assemblages can cause indirect demographic shifts throughout
prey communities even where numerical prey release and trophic
cascades are not apparent. While we predicted that predator-
induced demographic shifts would include growth rate (here
estimated by the parameter k), we found weak evidence for
changes in growth rate. Only the top predator, L. bohar and the
mid-level predator P. arcatus exhibited differences in the VBGF
parameter k, with the apex predator growing slower and the mid-
level predator growing faster at Palmyra, as predicted.
Estimates of maximum size (Linf) differed between islands for
most species, in agreement with our predictions. The apex
predator, L. bohar reached a significantly larger maximum size
and maximum age at Palmyra, likely a result of the current ban on
fishing in this U.S. National Wildlife Refuge and little extraction
for decades previously. In contrast, species from lower trophic
levels, including P. arcatus, P. dickii, and A. nigricans attained smaller
maximum sizes and had reduced longevity at Palmyra, where
overall top predator biomass is significantly greater [18,29] and
where predation pressure and/or predation risk is likely higher
than at Kiritimati . Our results complement the findings of
other studies of life history changes in coral reef fishes in response
to changes in predator abundance. Increases in apex predator
biomass were correlated with decreases in size at sex change of
many parrotfish species, when comparing the remote Northwest-
ern Hawaiian Islands with the heavily fished main Hawaiian
Islands  and when comparing four of the Northern Line
Islands across a gradient of human disturbance . Similar life
history shifts in the size at sex change have been reported in
Caribbean parrotfish in response to direct fishing pressure .
While fishing pressure is likely the strongest anthropogenic
impact that varies between these islands, differences in habitat,
coral disease, and microbial communities also exist. Coral cover is
higher at Palmyra than Kiritimati, while coral disease and
microbial concentrations are lower . Loss of live coral and
subsequent reduction in habitat complexity can lead to dramatic
changes in reef fish communities [30,48–50], including changes in
top predator biomass. Reductions in live coral and habitat
complexity on Kiritimati could further reduce abundance and
size of top predators, thereby increasing differences in predator
assemblages between islands and potentially increasing the
magnitude of indirect effects on lower trophic levels. However, it
is also likely that reductions of live coral cover and habitat
complexity would negatively impact lower trophic groups
dependent on those habitats and the shelter they provide
[48,49]. Still, our data cannot discount the possibility that
additional anthropogenic stressors may have contributed to the
patterns we observed.
Only C. margaritifer did not differ in Tmaxbetween islands, and
our estimate of Linfwas higher and k was lower for this species at
Palmyra than at Kiritimati, counter to our predictions. There are a
number of potential reasons why our predictions were unsupport-
ed for this species. First, as a planktivore, C. margaritifer may be
dependent on pelagic delivery of zooplankton. The bathymetry is
steeper and the currents often stronger at Palmyra than at
Kiritimati , possibly increasing the rate of delivery of
allochthonous zooplankton prey at Palmyra. Gut contents revealed
that C. margaritifer had eaten more calanoid (planktonic) copepods
compared to harpacticoid (benthic) copepods at Palmyra (E.
Madin, unpublished data), indicating a greater reliance on pelagic
prey. Changes in pelagic food supply could influence growth and
longevity, and possibly counter the effects of increased predation
pressure [13,52]. Additionally, methodological concerns may have
skewed results for C. margaritifer; for all other species, the relative
difference in size across islands was concordant between the in situ
count data (Fig. 2) and the collections (Fig. 3). In contrast, while
count data suggest that C. margaritifer are larger at Kiritimati, the
size distributions of our collections were indistinguishable
(Palmyra: 3.99 cm; Kiritimati: 3.98 cm; p.0.95). Based on
logistical constraints, our sampling methods for C. margaritifer
(unlike the other four species) were quite different at the two
islands: at Palmyra, we used BINCKE nets, which are more
effective at capturing larger individuals of benthic fishes , while
at Kiritimati we used clove oil, which is more effective at capturing
smaller individuals. Therefore, our collections of C. margaritifer may
not have been representative of populations at each island, which
in turn may have influenced the demographic patterns we
observed for this species.
A growing body of work has examined geographical variation in
demography for a variety of fish species . Many of these studies
have examined demographic and life history variation of non-target
species over large latitudinal scales, often attributing spatial
variation across 100 s to 1000 s of km to differences in temperature
[11,12,14,15]. In contrast, Palmyra and Kiritimati are separated by
less than 4u of latitude near the equator, and while Kiritimati
experiences slightly more tropical upwelling than Palmyra, water
temperatures generally differ by less than 1uC . Increased
tropical upwelling at Kiritimati also results in slightly higher
productivity there. However, recent work has demonstrated that
uninhabited, unfished equatorial atolls that experience as much or
more tropical upwelling than Kiritimati have values of total fish
biomass and top predator biomass that are similar to Palmyra and
different from Kiritimati [29,39]. Similar differences in regional
demographic parameters have been found in areas with tempera-
ture differences of 5–8uC and up to 10-fold differences in
productivity [13,14], environmental differences that are far greater
than those between Palmyra and Kiritimati. It is therefore most
likely that the changes in demography we have observed between
atolls in the Line Islands are the result of extensive inter-atoll
differences in predator assemblages driven by human exploitation
and not the result of environmental differences.
While differences in predator communities appear to have
strong demographic consequences throughout the food web, the
specific mechanisms by which longevity and size vary between
islands are still uncertain. Increases in predator abundance may
result in increased predation and direct increases in mortality of
prey species, they may influence behavioral changes of prey
species, or both. Behavioral changes may be related to prey
species’ assessment of predation risk while foraging, and can result
in behaviorally mediated trophic cascades [54,55]. Indeed, recent
work suggests that the behavior of many of our study species
changes between Palmyra and Kiritimati, such that prey spend
more time sheltering, less time foraging, and exhibit more
restricted movements at Palmyra where predators are more
abundant than at Kiritimati . Reductions in time spent
foraging should decrease the total amount of resources consumed,
which could in turn reduce the amount of energy available for
growth and reproduction [13,52]. Increases in predation risk may
also alter life history tradeoffs between growth and reproduction,
such that even less energy is allocated to growth and maintenance
. Additional evidence from these atolls suggest that species
from lower trophic groups are less robust (i.e., weigh less at a given
length) and have lower energy stores (i.e., relative liver size) at
Palmyra where predators are more abundant , in accordance
with life history theory. Our combined results suggest that
predator-induced demographic shifts may be more pervasive than
currently appreciated on coral reefs, and that the patterns we
observed on unfished Palmyra may be closer to the state of these
ecosystems before extensive human impacts.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org7June 2011 | Volume 6 | Issue 6 | e21062
parameter estimates for each species by island combination.
Reparameterized von Bertalanffy growth function
methods and results.
Reparameterized von Bertalanffy growth function:
We thank The Nature Conservancy, the U.S. Fish and Wildlife Service,
and the Palmyra Atoll Research Consortium for providing access and
logistical support on Palmyra; Kim Anderson of Dive Kiribati for logistical
support on Kiritimati; and K. Lafferty, C. McDonald, S. Smriga, J. Smith,
M. Vermeij, E. Madin, C. Lantz, R. McClintock, K. Ohlinger, J. Shaw
and A. Kuris with assistance in the field and in the laboratory. We thank C.
Mora and one anonymous reviewer for helpful comments on an earlier
draft of this manuscript.
Conceived and designed the experiments: SAS SLH BIR. Performed the
experiments: BIR SLH SMW MD AF ED ES SAS. Analyzed the data:
SAS BIR SLH. Wrote the paper: BIR SLH SAS.
1. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, et al. (2003)
Global trajectories of the long-term decline of coral reef ecosystems. Science 301:
2. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, et al. (2001)
Historical overfishing and the recent collapse of coastal ecosystems. Science 293:
3. Roberts CM (2007) The unnatural history of the sea. Washington, DC: Island
Press. 435 p.
4. Jennings S, Kaiser MJ, Reynolds JD (2001) Marine Fisheries Ecology. Oxford:
Blackwell. 417 p.
5. Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems.
Advances in Marine Biology 34: 201.
6. Hamilton SL, Caselle JE, Standish JD, Schroeder DM, Love MS, et al. (2007)
Size-selective harvesting alters life histories of a temperate sex-changing fish.
Ecological Applications 17: 2268–2280.
7. Hawkins JP, Roberts CM (2004) Effects of fishing on sex-changing Caribbean
parrotfishes. Biological Conservation 115: 213–226.
8. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish
communities. Nature 423: 280–283.
9. McClenachan L (2009) Documenting loss of large trophy fish from the Florida
Keys with historical photographs. Conservation Biology 23: 636–643.
10. Murawski SA, Rago PJ, Trippel EA (2001) Impacts of demographic variation in
spawning characteristics on reference points for fishery management. Ices
Journal of Marine Science 58: 1002–1014.
11. Choat JH, Robertson DR (2002) Age-based studies. In: Sale PF, ed. Coral Reef
Fishes: Dynamics and Diversity in a Complex Ecosystem. San Diego: Academic
Press. pp 57–80.
12. Robertson DR, Ackerman JL, Choat JH, Posada JM, Pitt J (2005) Ocean
surgeonfish Acanthurus bahianus. I. The geography of demography. Marine
Ecology Progress Series 295: 229–244.
13. Ruttenberg BI, Haupt AJ, Chiriboga AI, Warner RR (2005) Patterns, causes and
consequences of regional variation in the ecology and life history of a reef fish.
Oecologia 145: 394–403.
14. Meekan MG, Ackerman JL, Wellington GM (2001) Demography and age
structures of coral reef damselfishes in the tropical eastern Pacific Ocean. Marine
Ecology Progress Series 212: 223–232.
15. Trip EL, Choat JH, Wilson DT, Robertson DR (2008) Inter-oceanic analysis of
demographic variation in a widely distributed Indo-Pacific coral reef fish.
Marine Ecology Progress Series 373: 97–109.
16. Robertson DR, Choat JH, Posada JM, Pitt J, Ackerman JL (2005) Ocean
surgeonfish Acanthurus bahianus. II. Fishing effects on longevity, size and
abundance? Marine Ecology Progress Series 295: 245–256.
17. DeMartini EE, Friedlander AM, Holzwarth SR (2005) Size at sex change in
protogynous labroids, prey body size distributions, and apex predator densities at
NW Hawaiian atolls. Marine Ecology Progress Series 297: 259–271.
18. DeMartini EE, Friedlander AM, Sandin SA, Sala E (2008) Differences in fish-
assemblage structure between fished and unfished atolls in the northern Line
Islands, central Pacific. Marine Ecology Progress Series 365: 199–215.
19. Sandin SA, Walsh SM, Jackson JBC (2010) Prey release, trophic cascades, and
phase shifts in tropical nearshore marine ecosystems. In: Terborgh J, Estes JA,
eds. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature.
Washington, DC: Island Press. pp 71–90.
20. Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, et al.
(2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and
protected-area management. Environmental Conservation 27: 179–200.
21. Terborgh J, Estes JA, eds. (2010) Trophic Cascades: Predators, Prey, and the
Changing Dynamics of Nature. Washington, DC: Island Press. 488 p.
22. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, et al. (2002)
A cross-ecosystem comparison of the strength of trophic cascades. Ecology
Letters 5: 785–791.
23. Graham NAJ, Evans RD, Russ GR (2003) The effects of marine reserve
protection on the trophic relationships of reef fishes on the Great Barrier Reef.
Environmental Conservation 30: 200–208.
24. Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the
indirect effects of predator removal by exploitation. Ecology Letters 7: 410–416.
25. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O,
et al. (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate
change. Current Biology 17: 360–365.
26. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of
Caribbean coral reefs. Nature 450: 98–101.
27. Paddack MJ, Cowen RK, Sponaugle S (2006) Grazing pressure of herbivorous
coral reef fishes on low coral-cover reefs. Coral Reefs 25: 461–472.
28. Newman MJH, Paredes GA, Sala E, Jackson JBC (2006) Structure of Caribbean
coral reef communities across a large gradient of fish biomass. Ecology Letters 9:
29. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, et al. (2008)
Baselines and degradation of coral reefs in the Northern Line Islands. Plos One
30. Graham NAJ, McClanahan TR, MacNeil MA, Wilson SK, Polunin NVC, et al.
(2008) Climate warming, marine protected areas and the ocean-scale integrity of
coral reef ecosystems. PLoS One 3: e3039.
31. Conover DO, Munch SB, Arnott SA (2009) Reversal of evolutionary downsizing
caused by selective harvest of large fish. Proceedings of the Royal Society B-
Biological Sciences 276: 2015–2020.
32. Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass
of reef fishes between the northwestern and the main Hawaiian islands: the
effects of fishing down apex predators. Marine Ecology Progress Series 230:
33. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological
consequences of marine top predator declines. Trends in Ecology & Evolution
34. Robbins WD, Hisano M, Connolly SR, Choat JH (2006) Ongoing collapse of
coral-reef shark populations. Current Biology 16: 2314–2319.
35. Stallings CD (2009) Fishery-independent data reveal negative effect of human
population density on Caribbean predatory fish communities. Plos One 4:
36. Paddack MJ, Reynolds JD, Aguilar C, Appeldoorn RS, Beets J, et al. (2009)
Recent region-wide declines in Caribbean reef fish abundance. Current Biology
37. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, et al. (2008) Microbial
ecology of four coral atolls in the Northern Line Islands. Plos One 3: e1584.
38. Lafferty KD, Shaw JC, Kuris AM (2008) Reef fishes have higher parasite
richness at unfished Palmyra Atoll compared to fished Kiritimati Island.
Ecohealth 5: 338–345.
39. Williams ID, Richards BL, Sandin SA, Baum JK, Schroeder RE, et al. (2011)
Differences in reef fish assemblages between populated and remote reefs
spanning multiple archipelagos across the Central and Western Pacific. Journal
of Marine Biology Article ID 826234: 1–14.
40. Francis RICC (1988) Are growth-parameters estimated from tagging and age
length data comparable? Canadian Journal of Fisheries and Aquatic Sciences 45:
41. Burnham KP, Anderson DR (1998) Model selection and inference: a practical
information-theoretic approach. New York: Springer-Verlag. 353 p.
42. Kimura DK (1980) Likelihood methods for the von Bertalanffy growth curve.
Fishery Bulletin 77: 765–776.
43. R Development Core Team (2009) R: A language and environment for
statistical computing. Vienna, Austria. http://www.R-project.org: R Foundation
for Statistical Computing.
44. Walsh SM (2009) Linking coral reef health and human welfare [Ph.D.
Dissertation]. San Diego: University of California.
45. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population
control, and competition. American Naturalist 94: 421–425.
46. Power ME (1990) Effects of fish in river food webs. Science 250: 811–814.
47. Madin EMP, Gaines SD, Warner RR (2010) Field evidence for pervasive
indirect effects of fishing on prey foraging behavior. Ecology 91: 3563–3571.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org8 June 2011 | Volume 6 | Issue 6 | e21062
48. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, et al. (2006)
Dynamic fragility of oceanic coral reef ecosystems. Proceedings of the National
Academy of Sciences of the United States of America 103: 8425–8429.
49. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline
threatens fish biodiversity in marine reserves. Proceedings of the National
Academy of Sciences of the United States of America 101: 8251–8253.
50. Mora C (2008) A clear human footprint in the coral reefs of the Caribbean.
Proceedings of the Royal Society B-Biological Sciences 275: 767–773.
51. Hamann IM, Boehlert GW, Wilson CD (2004) Effects of steep topography on
the flow and stratification near Palmyra Atoll. Ocean Dynamics 54: 460–473.
52. Gust N, Choat JH, Ackerman JL (2002) Demographic plasticity in tropical reef
fishes. Marine Biology 140: 1039–1051.
53. Anderson TW, Carr MH (1998) BINCKE: a highly efficient net for collecting
reef fishes. Environmental Biology of Fishes 51: 111–115.
54. Beckerman AP, Uriarte M, Schmitz OJ (1997) Experimental evidence for a
behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the
National Academy of Sciences of the United States of America 94:
55. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-
mediated indirect interactions. Ecology Letters 7: 153–163.
56. Stearns SC (1992) The evolution of life histories. Oxford; New York: Oxford
University Press. xii, 249 p.
Demographic Shifts in Coral Reef Fish
PLoS ONE | www.plosone.org9 June 2011 | Volume 6 | Issue 6 | e21062