Download Distinguishing between direct and indirect effects of predators in

Journal of Animal Ecology 2013, 82, 438–448
doi: 10.1111/1365-2656.12001
Distinguishing between direct and indirect effects of
predators in complex ecosystems
Nessa E. O’Connor1,2*, Mark C. Emmerson1,2, Tasman P. Crowe3 and Ian Donohue4,5
1
School of Biological Sciences, Queen’s University Belfast, Northern Ireland, BT9 7BL, UK; 2Environmental Research
Institute, University College Cork, Cork, Ireland; 3School of Biology and Environmental Science, University College
Dublin, Belfield, Dublin 4, Ireland; 4School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland; and 5Trinity
Centre for Biodiversity Research, Trinity College Dublin, Dublin 2, Ireland
Summary
1. Global declines in biodiversity have stimulated much research into the consequences of
species loss for ecosystems and the goods and services they provide. Species at higher trophic
levels are at greater risk of human-induced extinction yet remarkably little is known about
the effects of consumer species loss across multiple trophic levels in natural complex ecosystems. Previous studies have been criticized for lacking experimental realism and appropriate
temporal scale, running for short periods that are not sufficient to detect many of the mechanisms operating in the field.
2. We manipulated the presence of two predator species and two groups of their prey (primary consumers) and measured their independent and interactive effects on primary producers in a natural marine benthic system. The presence of predators and their prey was
manipulated in the field for 14 months to distinguish clearly the direct and indirect effects of
predators on primary producers and to identify mechanisms driving responses.
3. We found that the loss of either predator species had indirect negative effects on species
diversity and total cover of primary producers. These cascading effects of predator species
loss were mediated by the presence of intermediate consumers. Moreover, the presence of different intermediate consumers, irrespective of the presence or absence of their predators,
determined primary producer assemblage structure. We identified direct negative effects of
predators on their prey and several indirect effects of predators on primary producers but not
all interactions could have been predicted based on trophic level.
4. Our findings demonstrate the importance of trophic cascade effects coupled with nontrophic interactions when predicting the effects of loss of predator species on primary producers and consequently for ecosystem functioning. There is a pressing need for improved
understanding of the effects of loss of consumers, based on realistic scenarios of diversity loss,
to test conceptual frameworks linking predator diversity to variation in ecosystem functioning
and for the protection of biodiversity, ecosystem functioning and related services.
Key-words: Algae, assemblage structure, biodiversity, crabs, ecosystem functioning, field
experiment, grazers, mussels, trophic cascade, whelks
Introduction
Given accelerating rates of species extinctions globally
(Pimm et al. 1995; Regan et al. 2001), predicting the consequences of species loss from ecosystems remains an elusive goal of critical importance (Loreau et al. 2001;
Hooper et al. 2005; Burkepile & Hay 2008; O’Gorman &
*Correspondence author. E-mail: [email protected]
Emmerson 2009). Understanding the consequences of loss
of species in complex, natural ecosystems requires that we
move beyond simple systems of competing species to
incorporate processes that occur across trophic levels
(Duffy et al. 2007; Stachowicz, Bruno & Duffy 2007).
Species at higher trophic levels are more at risk of
human-induced extinction (Duffy 2003; Estes et al. 2011)
yet relatively few studies have examined the effects of loss
of consumer diversity across multiple trophic levels in natural ecosystems (Worm et al. 2002; Duffy, Richardson &
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society
Distinguishing between direct and indirect effects of predators in complex ecosystems
France 2005; Byrnes, Reynolds & Stachowicz 2007; Duffy
et al. 2007; Bruno & Cardinale 2008; Burkepile & Hay
2008). The magnitude and direction of the effects of loss
of consumers are highly variable, probably determined by
the unique natural history of each species and may also
vary in different environmental contexts (Boyer, Kertesz &
Bruno 2009; O’Connor & Bruno 2009). The effects of
consumer species are difficult to predict because they
depend on many indirect, non-additive and behavioral
interactions (Sih, Englund & Wooster 1998; Byrnes,
Reynolds & Stachowicz 2007; Bruno & Cardinale 2008).
Whilst many studies have examined the relationship
between biodiversity and ecosystem functioning (Hooper
et al. 2005; Stachowicz, Bruno & Duffy 2007), few have
done so at appropriate experimental scales to capture a
realism that would enable current knowledge about the
functional roles of consumers to be incorporated into
ecosystem management (Bracken et al. 2008; Bruno &
Cardinale 2008; Naeem 2008a).
A growing number of studies have examined the intertrophic level effects of loss of species (Menge & Lubchenco
1981; O’Connor & Crowe 2005; Navarrete & Berlow
2006; Duffy et al. 2007; Stachowicz, Bruno & Duffy 2007;
Bruno & Cardinale 2008; Griffin et al. 2008). Few, however, have been designed to test for interactive effects of
loss of diversity within and among trophic levels (Bracken
et al. 2008; Bruno & Cardinale 2008; Naeem 2008a;
Mooney et al. 2010). Most factorial manipulations of
diversity at adjacent trophic levels to date were based on
plant-pollinators (Fontaine et al. 2006), laboratory-based
microbial systems (Naeem, Hahn & Schuurman 2000;
Fox 2004; Gamfeldt, Hillebrand & Jonsson 2005) or artificial experimental marine systems (Bruno & O’Connor
2005; Duffy, Richardson & France 2005; O’Connor &
Bruno 2007; Douglass, Duffy & Bruno 2008). Moreover,
the majority of this research is from short-term mesocosm
experiments which can only detect a subset of possible
mechanisms, lack sufficient environmental heterogeneity
to allow expression of niche differences and are of insufficient duration to capture population-level processes, such
as recruitment (Diaz et al. 2003; Srivastava & Vellend
2005; Stachowicz, Bruno & Duffy 2007; Bracken et al.
2008; Bruno & Cardinale 2008; Stachowicz et al. 2008a,
b). Experiments performed in spatially homogenous mesocosms also risk underestimating the value of species richness because spatial heterogeneity of the physical
environment plays a key role mediating the effects
of species diversity on ecosystem processes (Stachowicz
et al. 2008a,b; Griffin et al. 2009a; Crowe, Bracken & O’
Connor 2012).
Longer-term field experiments are accumulating and
have shown that the duration of a species loss experiment
is important in determining its outcome (O’Connor &
Crowe 2005; Navarrete & Berlow 2006; Stachowicz et al.
2008a). Experimental removals have shown that consumers
can have dramatic direct effects on lower trophic levels
(Paine 1976, 2002; Hawkins & Hartnoll 1983; O’Connor
439
& Crowe 2005; O’Connor et al. 2008; Edwards et al.
2010) even when interaction strengths are variable
(Navarrete & Berlow 2006). However, the indirect effects
of the loss of predators remain poorly understood
(Stachowicz, Bruno & Duffy 2007; Bruno & Cardinale
2008; Duffy 2009). Predators may affect primary producers indirectly by suppressing the activity of primary
consumers through density-dependent processes, such as
consumption (Silliman & Bertness 2002) or through traitmediated effects on primary consumers (Trussell et al.
2004), or directly by omnivory (Bruno & O’Connor 2005).
Changes in consumer abundance or behaviour can also
alter competitive interactions among species at different
trophic levels for other shared resources such as space
(Benedetti-Cecchi 2000). The direct and indirect (cascading) effects of loss of predators on lower trophic levels are
complex (Wootton 1994; Bruno & Cardinale 2008;
O’Gorman, Enright & Emmerson 2008) and experimental
manipulation is required to separate direct from indirect
effects. Field-based species removal experiments are an
additional tool that can be used to simulate the loss of
species from different trophic levels to further our understanding of the functional roles of consumers in ecosystems and to reveal the mechanisms by which biodiversity
affects ecosystem functioning in nature (Bracken et al.
2008; Stachowicz et al. 2008a,b; Edwards et al. 2010;
Crowe, Bracken & O’ Connor 2012).
We tested for effects of loss of species of predators and
their prey, both separately and together, on the diversity
and functioning of primary producers (macroalgae) on a
moderately exposed rocky shore. We manipulated two
common predatory species, whelks (Nucella lapillus) and
crabs (Carcinus maenas), and two groups of their primary
prey, mussels (Mytilus edulis) and grazing gastropods
(comprising primarily Patella vulgata, Littorina littorea
and Gibbula umbilicalis) (Fig. 1a), to identify and characterize the indirect effects of loss of predator species on
intertidal algal assemblages over 14 months. Only by
manipulating both predators and their prey separately can
we test clearly whether predators affect primary producers
directly (e.g. omnivory) or indirectly (e.g. mediated by
intermediate consumers) and investigate the mechanisms
involved (O’Connor & Bruno 2007; Mooney et al. 2010).
A crossed design of nine treatments (Fig. 1b) allowed us
to identify independent and interactive effects of predator
species and functional groups of their prey on total algal
cover and algal assemblage structure and diversity. To
help identify mechanisms driving the indirect effects of
predators on algae, we also examined interactions between
predator species (biomass) and their prey species (mussel
% cover, grazer biomass). Comparison of the two predator species would also highlight the occurrence of intraguild predation (Polis & Holt 1992). We examined
whether (i) the loss of predators or their prey affected the
structure or functioning of algal assemblages (measured
as total algal cover, diversity and assemblage structure
[i.e. a multivariate measure incorporating both species
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
440 N. E. O’Connor et al.
(a)
(b)
Fig. 1. (a) Simplified trophic interaction network of a moderately
exposed rocky shore (adapted from Little, Williams & Trowbridge 2009), with the components whose presence we manipulated and highlighted in red. While mussels may not interact
trophically with benthic macroalgae consistently, they can comprise important consumers of algal propagules (Santelices &
Martinez 1988) and can also have strong non-trophic interactions
with macroalgae arising primarily from competition for space on
the shore (Lubchenco & Menge 1978), which may also interact
with the presence of grazers (Crowe, Frost & Hawkins 2011).
Such strong non-trophic interactions are largely absent from food
web-based theoretical frameworks yet play a key role in determining the structure of algal assemblages. While crabs have been
found to feed on whelks (e.g. Hughes & Elner 1979), no predation by crabs upon whelks was observed during our experiment.
(b) Experimental design comprising nine treatments, involving
the removal of two species of predator and two groups of their
prey, to measure the independent and interactive effects of predators on primary producers and test for direct and indirect effects
across trophic levels.
composition and abundance]) and (ii) any effects were
species identity-dependent or could be predicted based
solely upon trophic level (i.e. whether both predators had
similar effects).
Materials and methods
experimental design
Our experimental site was located at Rush, Co. Dublin (53°31!4′
N, 6°04!9′W) on the east coast of Ireland on a moderately
exposed flat rocky reef containing networks of patches of bare
rock, mussels, barnacles and macroalgal stands typical of rocky
shores in the region (Appendix S1; O’Connor & Crowe 2008).
Our experimental design (Fig. 1b) was balanced with two fixed
factors: (i) ‘loss of predators’ (three levels: no predators removed,
whelks removed and crabs removed) and (ii) ‘loss of their prey
(primary consumers)’ (three levels: no primary consumers
removed, grazers removed and mussels removed). Whelks and
crabs are both highly susceptible to human impacts (Hawkins
et al. 2002; Sheehan et al. 2010), making them extremely pertinent for species loss experiments. Moreover, recent work has
indicated that the roles of mobile predators structuring European
rocky shore communities have not been fully recognized (Silva
et al. 2008). We incorporated the removal of mussels in our
experimental design because, although mussels were regarded as
basal species in some classic food web studies (e.g. Pimm 1980),
in fact algal propagules can comprise an important component of
mussel diet (Santelices & Martinez 1988), which may affect macroalgal settlement. Moreover, mussels are autogenic ecosystem
engineers (Jones, Lawton & Shachak 1997) and can drive strong
non-trophic interactions on rocky shores, potentially arising from
competition for space on rock surfaces (Lubchenco & Menge
1978). Mussels have also been shown to facilitate the presence of
certain algal species, and this may interact with grazing activity
(Crowe, Frost & Hawkins 2011). Thus, mussels are a source of
both strong trophic and non-trophic interactions, which should
be included in rocky shore interaction webs (Fig. 1a). For analyses of mussel cover and grazer biomass, there were only two levels of the factor ‘loss of primary consumers’ across the six
treatments in which they themselves were not manipulated. Similarly, there were two levels of the factor ‘loss of predators’ for
analyses of whelk biomass and crab biomass. Each treatment was
replicated four times.
Experimental plots were established within the mid- to low
shore. Each contained approximately 50% mussel cover prior to
the random allocation of treatments (range 45–55%). It was necessary to use cages to control the presence of mobile predators
and molluscan grazers. The cages consisted of square fences measuring 35 9 35 9 12 cm made of stainless steel mesh (0!9 mm
diameter, 3!33 mm aperture, 61% open area), allowing immigration and recruitment of primary producers and many epibenthic
consumers (including primary consumers and small predators,
e.g. amphipods, polychaetes and Nemertea). Our experimental
design, therefore, tested for effects of the local extinction of key
components of a larger intertidal food web, in an open experimental system without removing entire trophic levels (Fig. 1a).
To test for any experimental artefacts of the cages, we compared
algal and mussel cover and grazer biomass in experimental plots
without cages to the caged treatment within which all manipulated consumers were present. We found no difference in any of
these variables between the caged and uncaged treatments
(Appendix S2).
Experimental manipulations mimicked as closely as possible
natural patterns at the field site. Mussels and molluscan grazers
were removed manually from the treatments to simulate loss of
these species. Predators were added to the plots if required for
the treatment at a density of one individual per plot. In treatments where species were removed, there was no experimental
compensation for the loss of species, or artificial increase in biomass of remaining species, similar to an additive design (Byrnes
& Stachowicz 2009). Crabs found on the shore and used in the
experiment had a carapace width of 3–6 cm. This size range is
thought to feed mainly on mussels and small gastropods
(Rangeley & Thomas 1987), including limpets (Silva et al. 2008).
Although larger crabs may feed on whelks (Hughes & Elner
1979), no predation by crabs upon whelks was observed during
our experiment. Cages and treatments were checked regularly
(approximately every 2 weeks) and maintained during the experiment. Juveniles of species that were being excluded were removed
from the appropriate treatments as they became visible while settlement and recruitment of all other species was left intact. As
the experimental plots form part of a long-term study, we did not
take destructive samples to quantify the biomass of algae or mussels and instead quantified their percentage cover (O’Connor &
Crowe 2005; Martins et al. 2010). Algal cover and assemblage
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
Distinguishing between direct and indirect effects of predators in complex ecosystems
structure were quantified using a 64-point double-strung quadrat
(25 9 25 cm), which was placed in each plot, and all taxa under
each intersection point were recorded. Species within the quadrat
that did not match any intersection point were also recorded and
assigned a value of 1% cover. On these shores, it is not uncommon for total mean algal cover to be in excess of 100% owing to
the layered nature of benthic algae (encrusting, turfing, canopy
and epiphytic morphologies were all included). We calculated
taxon richness (number of taxa) and evenness (Simpson’s 1 " k)
as measures of algal diversity as recommended for diversity
manipulation experiments (Kirwan et al. 2007; Hillebrand,
Bennett & Cadotte 2008).
We quantified total interaction strengths between the manipulated consumers and algae over the duration of the experiment
based on the dynamic index (Laska & Wooton 1998) as:
lnðX!iþj =Xi"j Þ
Xj t
where X represents density of either prey (algal) species i
(expressed here in terms of percent cover) or consumer j (density
set equal to one). Prey species densities were quantified in the
presence, +j (calculated from the experimental treatment with no
species losses), or absence, "j, of consumer species j, whilst t represents time. We quantified interaction strengths only in experimental plots belonging to treatments from which the manipulated
consumers were removed in isolation. The experimental design
employed here did not permit the calculation of direct per capita
effects. Rather, we used the resulting values to provide an estimate of the net effect of consumer j on algal per cent cover in
the treatments over the duration of the experiment (O’Gorman
et al. 2010). The effects detailed here for predators therefore represent indirect effects of the predators on algal per cent cover
mediated by their impact on intermediate consumers.
statistical analyses
Data were examined for normality, and analysis of variance (ANOwas used to test hypotheses involving algal and mussel cover
and grazer, crab and whelk biomass after first testing for
homogeneity of variances with Cochran’s test. Variables were
transformed where necessary to homogenise variances. The
Student–Newman–Keuls procedure was used to make post-hoc
comparisons among levels of significant terms. Permutational
multivariate analysis of variance (PERMANOVA; Anderson
2001; McArdle & Anderson 2001) was used to test hypotheses
about algal assemblage structure. Non-metric multidimensional
scaling (MDS) was used to produce two-dimensional ordinations
to compare algal assemblages among different treatments (Field,
Clarke & Warwick 1982; Clarke 1993). SIMPER (Similarity of
Percentages; Clarke & Warwick 2001) analyses were used to identify which algal taxa contributed most to pairwise dissimilarities
between treatments. All multivariate analyses were based on
Bray-Curtis similarity matrices calculated from log (x + 1)-transformed per cent cover data and were performed with 9999
permutations of the residuals under a reduced model with PRIMER
Version 6.1.10 (PRIMER-E Ltd., Plymouth, UK).
VA)
Results
When all consumer species were present in an experimental plot, the mean total algal cover was 78!5% (SE ±24)
441
(Fig. 2a). Effects of predator species loss on algal cover
(Fig. 2a), taxon richness (Fig. 2b) and evenness (Fig. 2c)
were mediated by the presence or absence of intermediate
species, shown by significant interactions between loss of
predators and loss of primary consumers (algal cover:
MS = 3704!08, F4,27 = 3!02, P = 0!035; taxon richness:
MS = 7!53, F4,27 = 3!78, P = 0!014; evenness: MS = 0!13,
F4,27 = 4!56, P = 0!006). The removal of either species of
predator alone (crabs or whelks) reduced total algal cover
and both measures of algal diversity (P < 0!05 in all
cases), whereas there was no distinguishable effect of any
of the other treatments (Fig. 2). Further, the loss of crabs
in isolation reduced algal taxon evenness more than when
only whelks were lost (P < 0!05; Fig. 2c). Both predators
had significant negative indirect effects on total algal
cover and diversity of algal assemblages, but only when
primary consumers were present. Surprisingly, the loss of
primary consumers either alone or in combination with
the loss of a predator had no effect on total algal cover,
taxon richness or evenness of algal assemblages (Fig. 2).
In terms of interaction strengths, both grazers
("1!31 ± 0!07;
mean ± SE,
n = 4)
and
mussels
("1!42 ± 0!09) had similar total interaction strengths with
their algal prey, as did whelks (1 ± 0!8) and crabs
(1!39 ± 0!76).
The multivariate structure of algal assemblages was not
affected by the loss of predators (MS = 2105!20, pseudoF2,27 = 1!15, P = 0!30), but rather was altered significantly
following the loss of primary consumers (MS = 19510,
pseudo-F2,27 = 10!8, P & 0!0001; Fig. 3). Pairwise tests
showed that the loss of grazers (grazers present versus
grazers removed: pseudo-t = 1!98, P < 0!001) and the loss
of mussels (mussels present versus mussels removed:
pseudo-t = 2!97, P & 0!0001) both altered algal assemblage structure, although in significantly different ways
(grazers removed versus mussels removed: pseudot = 6!31, P & 0!0001). The removal of mussels resulted in
a shift in dominance towards red algae such as crustose
algae ‘Lithothamnia’ spp., Osmundea spp., Chondrus crispus (possibly incorporating some Mastocarpus stellatus)
and Corallina officianalis, while assemblages without grazing gastropods were dominated by brown and ephemeral
algae such as Fucus serratus, Porphyra umbilicalis and
Ulva spp. (Appendix S3).
The local extinction of whelks resulted in a significant
increase in the biomass of crabs (MS = 49!88,
F1,18 = 5!17, P = 0!036; Fig. 4a), whereas the loss of either
group of primary consumers had no effect on crab biomass (MS = 15!5, F2,18 = 1!61, P = 0!23). In contrast, we
did not detect any difference in whelk biomass in any of
the treatments involving removal either of their prey or
crabs (Appendix S4; Fig. 4b). There was, however, a significant interaction between the loss of predators and the
loss of grazers on mussel cover (MS = 1938!54,
F2,18 = 10!02, P = 0!001). The removal of whelks or crabs
in isolation led to increased mussel cover, whereas the loss
of grazers, either in isolation or in combination with the
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
442 N. E. O’Connor et al.
(a)
(b)
(c)
Fig. 2. (a) Total cover, (b) taxon richness (number of taxa) and (c) taxon evenness (Simpson’s 1 " k) of algae in each experimental
treatment. Values are untransformed means (±SE, n = 4). Letters (a–c) indicate groups that are statistically indistinguishable from each
other (P > 0!05).
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
Distinguishing between direct and indirect effects of predators in complex ecosystems
443
mussels on grazer biomass (MS = 14!81, F2,18 = 22!1,
P & 0!0001; data were square-root transformed). The
loss of either predator species, in combination with the
loss of mussels, led to an increase in grazer biomass
(P < 0!01; Fig. 4d).
Discussion
Fig. 3. Non-metric multidimensional scaling (MDS) ordination
of algal assemblages in each experimental treatment based on a
Bray–Curtis similarity matrix calculated from log (X + 1)-transformed algal cover data (stress = 0!18). Open symbols represent
plots with all primary consumers present, grey symbols represent
plots that had grazing gastropods removed, and filled symbols
represent plots that had mussels removed.
loss of either predator species, reduced mussel cover significantly (P < 0!01; Fig. 4c). There was also a significant
interaction between the loss of predators and loss of
Our results demonstrate clearly that species at intermediate trophic levels regulate the cascading effects of predators on primary producers and highlight the importance
of indirect effects in natural ecosystems. Loss of either of
the two common predators we manipulated had negative
indirect effects on the total cover and diversity of benthic
primary producers. However, these effects were mediated
by the presence of species in an intermediate trophic level
and, moreover, different functional groups of these intermediate species determined different assemblages of primary producers. Specifically, the loss of whelks or crabs
led to a reduction in total algal cover and diversity (both
(a)
(b)
(c)
(d)
Fig. 4. (a) Crab biomass, (b) whelk biomass, (c) mussel cover and (d) grazer biomass in the experimental treatments containing these
consumers. Inset in (a) shows the overall main effect of whelk removal on crab biomass. Values are untransformed means (±SE, n = 4).
Letters (a–c) indicate groups that are statistically indistinguishable from each other (P > 0!05).
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
444 N. E. O’Connor et al.
taxon richness and evenness), but only when intermediate
trophic levels (their prey) were intact. In addition, the loss
of one group of their prey, mussels, led to a shift towards
dominance of red algae, whereas the loss of another
group of their prey, grazing gastropods, led to the dominance of brown and ephemeral algae. We have, therefore,
identified several cascading effects of predators on primary producers. Not all of these could have been predicted based on trophic level alone because the different
groups of their prey had different effects on primary producers that may or may not be related to trophic interactions (e.g. mussels may compete with some algal species
for space or facilitate the establishment of other algal species (Lubchenco & Menge 1978; Crowe, Frost & Hawkins
2011). Our results demonstrate the importance of cascading effects of predators coupled with knowledge of the
functional roles of intermediate species when predicting
the indirect effects of loss of predators on ecosystem processes such as primary production.
Previous studies of marine benthic predators concluded
that predator effects were probably non-additive, antagonistic interactions or emergent predator effects that operate at larger spatial or temporal scales than included in
most short duration experiments (Leroux & Loreau 2009;
O’Connor & Bruno 2009). We found that the loss of
either predator species affected their prey positively (mussels directly; grazers when combined with the loss of mussels), even though an alternative predator was always
present. Therefore, neither species appears to compensate
for the loss of the other, suggesting that their combined
effects on their prey may be additive. However, further
manipulations of predator diversity are required to test
this explicitly (Sih, Englund & Wooster 1998). Interestingly, whelks were not affected by the loss of crabs or
either prey group. However, the loss of whelks led to an
increase in crab biomass, indicative of inter-specific competition between whelks and crabs and suggesting that
whelks may outcompete crabs for their shared prey. This
was a surprising result, considering that crabs have been
shown to prey on whelks (Kitching, Muntz & Ebling
1966; Hughes & Elner 1979). However, we found no
evidence of this during the experiment.
Further complications can be expected to occur when
the effects of loss of predators are density dependent, vary
with the presence of other species at different trophic levels, or vary with evenness of the consumer species (Griffin
et al. 2008; O’Connor et al. 2008). Previous work on
predatory crabs has shown that some species can compensate for the removal of key predators, but these effects
were density dependent (O’Connor et al. 2008). Our
results show that it is necessary to consider the role of the
species present across trophic levels to predict the effects
of loss of predators. For example, the loss of either crabs
or whelks led to a dramatic reduction in total algal cover,
indicating that both species play a similar role in terms of
their indirect effects on algae, consistent with their interaction strengths. However, the mediation of this indirect
effect varied significantly with the presence of different
intermediate consumers. When either predator was
removed in isolation, mussel cover increased, and this
appears to have been facilitated by the presence of grazers
as indicated by the decrease in mussel cover when grazers
were removed, probably caused by grazers removing algal
propagules that ultimately compete with the mussels for
space. This positive interaction, or facilitation, between
grazers and mussels is important for the continued existence of mussels and negated any negative effect of crabs
or whelks on mussel cover. In contrast, only the combined removal of either predator with mussels led to an
increase in grazer biomass, possibly because the combination of reduced predation pressure and increased availability of space following removal of mussels allowed for
greater algal production providing optimal feeding conditions for grazers.
Despite decades of research, the key processes determining community structure on rocky shores are not
understood fully and our findings draw together two paradigms. In Europe, strong grazer control of algal communities has long been known (Jones 1948; Hawkins 1981;
Jenkins et al. 2005; O’Connor & Crowe 2005; Coleman
et al. 2006; Jonsson et al. 2006), whereas on the east coast
of North America where patellids are absent, competitive
interactions among key space holders mediated by predation are considered key to understanding how the system
functions (Jenkins et al. 2008). Here we show that a combination of cascading predation effects, competitive interactions and direct consumption regulate algal
assemblages, but the exact mechanism determining species
presence and abundance varies among algal species.
Although the cumulative effects of consumers have
been shown to affect prey populations (e.g. Lubchenco &
Menge 1978; Menge & Lubchenco 1981; Rilov & Schiel
2006; O’Connor et al. 2011), separating the effects of different species and types of consumers has proven difficult
(Edwards, Conover & Sutter 1982; Menge 1982). It is
widely accepted that N. lapillus has a strong regulatory
role on the abundance of filter feeders such as mussels
and barnacles (Connell 1961; Menge 1976; Petraitis 1987)
and that C. maenas is an opportunistic scavenger, preying
on mussels (Kitching, Sloane & Ebling 1959; Bertness
et al. 2004), barnacles (Burrows, Kawai & Hughes 1999),
littorinids (Janke 1990), limpets (Griffin et al. 2008; Silva
et al. 2008, 2010) and whelks (Kitching, Muntz & Ebling
1966). The generality of the indirect effects of these predators on algae were, however, previously unclear. On
American Atlantic shores, it has been argued that C. maenas (where it is an invasive non-native species) has a positive indirect effect on the abundance of algae by
suppressing herbivore (mainly L. littorea) and whelk populations (Lubchenco & Menge 1978; Lubchenco 1983).
Although there is some controversy surrounding the evolution of L. littorea, it now seems most probable that it is
also non-native on west Atlantic shores (Reid 1996; Wares
et al. 2002; Chapman et al. 2007; Cunningham 2008;
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
Distinguishing between direct and indirect effects of predators in complex ecosystems
Brawley et al. 2009). Further, studies have shown that the
presence of C. maenas affects the behaviour of littorinids
and whelks leading to a trait-mediated indirect effect on
algal populations (Trussell, Ewanchuk & Bertness 2002,
2003). In contrast, in Europe, the effects of predation on
the dominant grazers, limpets, have only been demonstrated recently (Griffin et al. 2008; Silva et al. 2008,
2010) and, until now, there was extremely limited evidence
of indirect effects of predators on algal assemblages. This
led to suggestions that C. maenas may have a much
reduced role in indirect control of algal populations than
in the western Atlantic owing to differences in vulnerability of dominant grazers (Jenkins et al. 2008; Silva et al.
2010). Our results suggest the opposite because, although
the cages we used also excluded other potentially important predators, such as other crabs and birds (Coleman
et al. 1999; Silva et al. 2010), the fact that algal and mussel cover and grazer biomass in (uncaged) control plots
did not differ from that of plots that had cages and both
predators present, indicating that both N. lapillus and
C. maenas are key predators driving direct and indirect
effects in this system.
Our study demonstrates clearly that the loss of a predator (C. maenas or N. lapillus) has indirect positive effects
on total algal cover. However, this effect was mediated
via different mechanisms than predicted for American
shores. This may be due to the dominance of patellid limpets, rather than littorinids, as key grazers in Europe
(Jones 1948; Hawkins 1981; Jenkins et al. 2005; O’Connor
& Crowe 2005; Coleman et al. 2006; Jonsson et al. 2006)
or because algal populations on North American shores
are dominated by C. crispus (Lubchenco & Menge 1978)
and M. stellatus, whereas European shores comprise of
mixtures of algal taxa that include F. serratus (barely
present on western Atlantic), as well as Osmundea spp.,
C. crispus and M. stellatus (Jenkins et al. 2008; Brawley
et al. 2009). We show that the network of patches of mussels, fucoid and red algal stands, typical of moderately
exposed rocky shores in this region, results from the
direct effects of predators on grazers, which determine the
fucoid dominance, and on mussels, which determine red
algal dominance. Thus, it is necessary to understand the
interactions among mussels, grazers and algae to predict
the effects of loss of predators on ecosystem functioning.
We found that predator removals led to increases in
their prey and subsequent shifts in algal composition.
These different algal assemblages have important implications for the functioning and stability of the system
because different algal taxa may perform differently in
terms of primary and secondary productivity (Bruno et al.
2008). For example, trade-offs exist so that rates of net
primary productivity may vary depending on the palatability of the primary producer (Bruno et al. 2005; Griffin
et al. 2009b).
Recent studies have challenged the presumption that
predator species cause qualitatively similar kinds of indirect effects in ecosystems (Chapin et al. 1997; Loreau
445
et al. 2001; Schmitz 2008). Schmitz (2008) showed that
two predator spider species with different hunting modes
(actively hunting versus sit-and-wait) had different indirect effects on primary producers (diversity and functioning) mediated by an intermediate prey species
(grasshopper). These species-specific identity effects
emerged as predators altered plant assemblage composition and showed that trait-based functions, such as hunting modes, could be used to predict the effects of
predators. Our experiment expanded this approach by
testing for effects of two phylogenetically, morphologically and behaviourally different predator species (with
very different hunting modes) on their prey, while simultaneously testing for interactions between the predators
across trophic levels and including whole prey assemblages (intermediate species and primary producers). In
contrast, our results show that although we found evidence of some intra-guild predator interactions (whelks
had a negative effect on crab biomass), both predators
had similar direct effects on their prey (grazers and mussels) and indirect effects on algae, suggesting that neither
predator functional traits nor species identity were
required to predict the effects of loss of benthic predators
in this system. However, the identity of intermediate consumers determined algal assemblage structure; therefore,
more empirical research examining the multi-trophic
effects of loss of consumers is required to undertake phylogenetic and trait-based forecasting of biodiversity effects
for ecosystem functioning (Naeem 2008b; Schmitz 2009).
general methodological caveats
There are several complicating factors to consider when
attempting to identify and characterise the direct and indirect effects of predator species loss. It is also important to
consider that there are several approaches to investigating
the effects of loss of consumers, each employing different
experimental designs that may pre-determine the likelihood of detecting certain interactions (Byrnes &
Stachowicz 2009). We have chosen to mimic the local
extinction of several species of consumer at different trophic levels so that we could test for interactions across
trophic levels and identify potential species-specific effects
within trophic levels. An important next step would be to
test whether such interactions are density dependent
which could be addressed using a substitutive design (e.g.
O’Gorman, Enright & Emmerson 2008; Griffin et al.
2010) or a combination of additive and substitutive
designs to test explicitly for compensation effects of
remaining species (e.g. O’Connor & Crowe 2005;
O’Connor et al. 2008). Another useful, albeit logistically
challenging, advancement would be to test whether other
species not considered explicitly as part of this study
could provide a level of biological insurance and whether
these remaining species are likely to increase in response
to the loss of species. The use of cages will nearly always
introduce certain caveats. For example, the density of
© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448
446 N. E. O’Connor et al.
enclosed species may not be completely representative of
how they would respond in an entirely open system
following species loss. However, careful controls can limit
this (Underwood 1980; Benedetti-Cecchi & Cinelli 1997;
Miller & Gaylord 2007). Finally, the duration of this
study was considerably longer than most marine biodiversity–ecosystem functioning experiments (Crowe, Bracken &
O’ Connor 2012). However, more studies over even longer
periods are required to assess the degree to which species
are ecologically redundant (Stachowicz, Bruno & Duffy
2007).
conclusion
Our findings demonstrate that, in order to advance an
understanding of the role of predators in ecosystems, we
must simultaneously consider non-additive and nontrophic interactions of consumers in addition to their
direct effects through local prey consumption and their
indirect effects on lower trophic levels (Leroux & Loreau
2009). It is essential that future empirical studies are
conducted over longer periods than many previous biodiversity experiments, are open to processes such as
dispersal and recruitment, include naturally heterogeneous
substrates and environmental conditions and are based on
realistic estimates of diversity change (Srivastava &
Vellend 2005; Stachowicz, Bruno & Duffy 2007; Bracken
et al. 2008; Stachowicz et al. 2008a; Crowe, Bracken & O’
Connor 2012). There are extremely few studies, such as
the experiment described here, that have attempted to
mimic the removal of several species from different
trophic levels simultaneously in the field. We argue that
the next step is to test the context-dependency of these
results preferably under different environmental conditions aligned with predicted global change scenarios. Such
studies are essential to test conceptual frameworks linking
predator diversity to species loss and variation in ecosystem functioning (Bruno & Cardinale 2008; Schmitz 2009),
an essential step to making realistic predictions of effects
of species loss that may be tested across ecosystems
(Naeem 2008a,b).
Acknowledgments
This work was funded by an Irish Research Council for Science, Engineering and Technology (IRCSET) Embark Postdoctoral Fellowship and an
EPA Ireland STRIVE Fellowship (2007-FS-B-8-M5) to N. E. O’Connor
and an EPA Ireland STRIVE grant to I. Donohue (2008-FS-W-7-S5).
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Received 14 March 2012; accepted 1 September 2012
Handling Editor: Guy Woodward
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Appendix S1. Description of the experimental site.
Appendix S2. ANOVA tests for experimental artefacts of the cages
used to simulate the local extinction of target consumers.
Appendix S3. Results of SIMPER analyses identifying the taxa
contributing most strongly to differences in algal assemblage
structure following the loss of primary consumers.
Appendix S4. ANOVA test for effects loss of crabs, grazers and
mussels, both separately and together, on whelk biomass.
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© 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society, Journal of Animal Ecology, 82, 438–448