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robustness of natural food webs [8], even though
dynamic models clearly indicate the importance of
top-down and horizontal indirect effects among species
in propagating extinction cascades [9–11]. Currently,
there is little empirical evidence for secondary extinctions
being caused by the loss of positive indirect interactions
following a primary extinction, despite evidence that
indirect interactions play a dominant role in structuring
ecological communities [12].
Species at higher trophic levels (carnivores) are particularly vulnerable to extinction [1], and positive
indirect interactions among these species have long
been considered a potentially important mechanism
for the maintenance of species diversity [13– 16].
Competition between resource species can lead to an
indirect mutualism between their consumers [16,17],
because a consumer that reduces the density of its
prey also reduces competition at the prey’s trophic
level with positive effects on other prey species and,
thereby, their consumers. Consequently, the extinction
of one carnivore species could lead to cascading extinctions of other carnivores whose prey are outcompeted
by the prey that is released from top-down control.
Indirect mutualism can occur when consumer species
are sufficiently specialized, with each feeding predominantly on different food resources [13]. Despite the
potential importance of this effect, empirical evidence
for it is scarce and either based on observations of
co-occurrence patterns of aquatic predators [15] or
experimental studies of interactions among herbivores
on a rocky shore [14] and granivores in a desert ecosystem [18], both of which have problems associated with
their experimental design [19,20].
Communities of plants, insect herbivores and insect
parasitoids account for a large part of the Earth’s
species and are characterized by a high degree of diet
specialization [21]. Furthermore, they have proved to
be excellent experimental models for food web ecology
[22– 24]. We assembled replicate communities consisting of plants as a shared resource for two aphid species
and two parasitoid wasps each of which attacks only
one of the aphid species. We hypothesized that exclusion of either parasitoid species would have a
negative effect on the population of the other as a
result of increased resource competition between
their respective host species. We show that the absence
of one parasitoid species leads to the extinction of the
other and that this effect is transmitted through four
trophic links.
Biol. Lett. (2012) 8, 960–963
doi:10.1098/rsbl.2012.0572
Published online 15 August 2012
Community ecology
Indirect
commensalism
promotes persistence of
secondary consumer
species
Dirk Sanders1,2 and F. J. Frank van Veen1,*
1
Centre for Ecology and Conservation, College of Life and
Environmental Sciences, University of Exeter, Cornwall Campus,
Penryn, Cornwall TR10 9EZ, UK
2
Community Ecology, Institute of Ecology and Evolution, Baltzerstrasse 6,
3012 Bern, Switzerland
*Author for correspondence ( [email protected]).
Local species extinctions may lead to, often unexpected, secondary extinctions. To predict these,
we need to understand how indirect effects,
within a network of interacting species, affect
the ability of species to persist. It has been
hypothesized that the persistence of some predators depends on other predator species that
suppress competitively dominant prey to low
levels, allowing a greater diversity of prey species,
and their predators, to coexist. We show that, in
experimental insect communities, the absence
of one parasitoid wasp species does indeed lead
to the extinction of another that is separated by
four trophic links. These results highlight the
importance of a holistic systems perspective
to biodiversity conservation and the necessity to
include indirect population dynamic effects in
models for predicting cascading extinctions
in networks of interacting species.
Keywords: aphids; indirect effects; food web;
parasitoid; resource competition; secondary
extinctions
1. INTRODUCTION
Owing to the interdependence of species in ecosystems, biodiversity loss as a result of human activities
may lead to cascades of secondary extinctions [1 – 4].
Predicting these extinctions is often difficult and
requires an understanding of the mechanisms by
which the effects of the loss of one species are transmitted through the network of interactions among
species [5]. Models of secondary extinctions in food
webs (networks of trophically interacting species) can
be divided into two classes: (i) topological models
that only consider network structure, and in which
extinctions happen when species no longer have any
resources and (ii) dynamic models in which population
dynamics of all species are governed by their interactions.
The limitations of the first class are commonly acknowledged, chief among these being that they do not allow
for top-down effects and competitive interactions [6,7].
Nevertheless, they are still often applied to test the
2. MATERIAL AND METHODS
Experimental communities were assembled from Vicia faba (L) (var.
the Sutton) plants as a shared resource for the herbivorous aphids
Aphis fabae (Scopoli) and Acyrthosiphon pisum (Harris) and the parasitoid wasps Lysiphlebus fabarum (Marshall) and Aphidius ervi
(Haliday), each of which attacks only one of the aphid species.
Experimental cages were arranged in seven blocks, each containing
one cage of each experimental treatment (figure 1a): (i) both the
parasitoid species L. fabarum and Aphidius ervi present, (ii) only
L. fabarum present, and (iii) only Aphidius ervi present. The plant
V. faba and the aphid species Acyrthosiphon pisum and Aphis fabae
were present in all treatments.
Communities were contained in 30 30 30 cm Plexiglas cages
with a fine mesh sleeve for ventilation and access. Each cage contained eight 9 cm diameter pots with four V. faba plants each. The
plants were renewed by twice a week replacing the two oldest pots
with fresh ones containing two-week old seedlings, taking care to
return all insects to the cage. This procedure allows the long-term
maintenance of experimental aphid populations, with a carrying
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2012.0572 or via http://rsbl.royalsocietypublishing.org.
Received 15 June 2012
Accepted 26 July 2012
960
This journal is q 2012 The Royal Society
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Indirect commensalism among carnivores D. Sanders and F. J. F. van Veen
(a)
I L. fabarum
A. ervi
A. fabae
II L. fabarum
A. pisum
III
A. fabae
V. faba
A. pisum
A. ervi
A. fabae
V. faba
(b) 100
961
A. pisum
V. faba
(c) 200
Lysiphlebus fabarum
Aphidius ervi
80
individuals
150
60
100
40
50
20
0
0
(d) 4000
(e) 3000
Aphis fabae
Acyrthosiphon pisum
2500
3000
individuals
2000
2000
1500
1000
1000
500
0
0
1
2
3
4
5
6
7
8
week
1
2
3
4
5
6
7
8
week
Figure 1. Population dynamics in the experimental insect communities. (a) Compositions of the three experimental community
treatments (seven replicates of each). (b–e) Densities of the four insect species during the eight weeks of the experiment in
treatments with both parasitoid species (purple diamonds), L. fabarum only (red circles) and Aphidius ervi only (blue triangles).
Values are the means of the seven replicates in each treatment and error bars represent + s.e.m.
capacity in the order of 2000–3000 individuals, but does not prevent
interspecific competition [24]. The experimental cages were kept in a
controlled environment room at 208C, relative humidity 75 per cent,
with a 16 L : 8 D cycle. Under these conditions, the generation times
are 9 and 12 days for the aphids and parasitoids, respectively.
At the start of the experiment, five wingless adult females of each
aphid species were introduced (both species reproduce asexually by
giving birth to live female young under summer conditions). Ten
days after the aphids, three mated female parasitoids were released
for each species as per experimental treatment. The parasitoid
females lay eggs in immature aphids and the wasp larvae feed internally on their host before killing it and pupating inside the dried skin
of the host, forming a so-called ‘mummy’. Only a single parasitoid
individual can develop per host individual so the number of mummies in a cage can be used as a measure of population density.
Once a week, during the eight weeks of the experiment, the
number of aphids and parasitoid mummies of each species was
counted on half of the plants in each cage.
Biol. Lett. (2012)
The responses of aphid and parasitoid populations to the experimental treatments were analysed using linear mixed-effects models
with log transformed cumulative (over time) density data as response
variable. The effect of experimental treatment on the population size
of each species was tested as fixed effect with ‘block’ included as
random effect. Significance levels were determined by comparing
models with and without the treatment effect using maximumlikelihood methods. Analysis was carried out using the open source
software R v. 2.13.2 [25].
3. RESULTS
The parasitoid L. fabarum showed lower population
densities (figure 1b; likelihood-ratio (LR) ¼ 9.44,
p , 0.01), and went extinct in all seven replicates
within six weeks (two to three generations; figure 2a),
Downloaded from http://rsbl.royalsocietypublishing.org/ on June 15, 2017
962 D. Sanders and F. J. F. van Veen
(a)
Indirect commensalism among carnivores
(b)
Lysiphlebus fabarum
1.0
proportion of replicates persisting
proportion of replicates persisting
1.0
Aphidius ervi
0.8
0.6
0.4
0.2
0
0.8
0.6
0.4
0.2
0
2
3
4
5
week
6
7
8
2
3
4
5
week
6
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Figure 2. Persistence of experimental parasitoid populations. (a) L. fabarum in the presence (purple diamonds) and absence
(red circles) of Aphidius ervi. (b) Aphidius ervi in the presence (purple diamonds) and absence (blue triangles) of L. fabarum.
when Aphidius ervi was omitted from the community.
In contrast, L. fabarum persisted in all replicates in
the presence of Aphidius ervi. These differences were
associated with lower population densities, and eventually extinction, of Aphis fabae (the host of
L. fabarum) (figure 1d, LR ¼ 9.73, p , 0.01) and
markedly higher population densities of Acyrthosiphon
pisum (figure 1e, LR ¼ 17.18, p , 0.0001) in the
absence of the parasitoid Aphidius ervi.
We found no evidence for a reciprocal positive effect
of L. fabarum on Aphidius ervi (figure 1c, LR ¼ 3.29,
p . 0.05) and there was no difference in population
persistence of the latter between the treatments
(figure 2b). There was a clear effect of the presence
of L. fabarum on the population of its host Aphis
fabae (figure 1d, LR ¼ 7.32, p , 0.01), but this
did not affect the density of Acyrthosiphon pisum
(figure 1e, LR ¼ 2.63, p . 0.1).
4. DISCUSSION
We found a clear positive indirect effect of the parasitoid Aphidius ervi on another parasitoid, L. fabarum,
via four trophic links (figure 1a), such that populations
of L. fabarum could only persist in the presence of
Aphidius ervi. The extinction of L. fabarum was a
result of the extinction of its host, Aphis fabae, through
competitive exclusion by the aphid Acyrthosiphon
pisum, when the latter species was not controlled by
its parasitoid. Our experiment demonstrated that consumer species whose prey compete for a shared resource
can have a strong positive indirect effect on each
other, promoting species persistence at the resource
and the consumer level. Therefore, when considering
this mechanism, species losses can indeed lead to secondary extinctions of indirectly linked species.
We found no evidence for a reciprocal effect of
L. fabarum on Aphidius ervi. Acyrthosiphon pisum (the
host of Aphidius ervi) populations were only regulated
by their parasitoid and not by interspecific resource
competition, and hence there was no scope for indirect
Biol. Lett. (2012)
effects to be transmitted in this direction. This asymmetry in competition among the two aphid species
led to an indirect commensalism between the parasitoid species, rather than the expected indirect
mutualism. We have observed such strongly asymmetric competition among aphids before [24] but the
underlying mechanisms remain unclear. In general,
competition is typically asymmetric [26] so that indirect commensalism should be more frequently found
than indirect mutualism.
We conclude that secondary consumer species whose
prey compete for a shared resource can indeed have a
strong positive indirect effect on each other, promoting
population persistence and the maintenance of biodiversity. Loss of this positive indirect effect, through the
removal of one species, can lead to the extinction of
another species that is four trophic links removed. Our
experimental communities were very simple and in
natural diverse and complex communities there are
likely a number of other indirect pathways that either
reduce or strengthen the effect identified here. Moreover, in spatially structured communities the degree of
competition could vary in space and allow for recolonization following local extinctions. These results
emphasize the necessity for including population
dynamic effects in food web models aimed at testing
the robustness of natural multitrophic communities to
primary extinctions [27]. Current species extinctions
are biased towards higher order consumers [1] which,
by the mechanism demonstrated here, could lead to a
cascade of secondary extinctions.
D.S. was supported by Deutsche Forschungsgemeinschaft
grant no. SA 2003/1-1. University of Exeter BIO2407
(2011) students assisted with data collection.
1 Borrvall, C. & Ebenman, B. 2006 Early onset of secondary extinctions in ecological communities following the
loss of top predators. Ecol. Lett. 9, 435–442. (doi:10.
1111/j.1461-0248.2006.00893.x)
2 Borrvall, C., Ebenman, B. & Jonsson, T. 2000 Biodiversity lessens the risk of cascading extinction in model food
Downloaded from http://rsbl.royalsocietypublishing.org/ on June 15, 2017
Indirect commensalism among carnivores D. Sanders and F. J. F. van Veen
3
4
5
6
7
8
9
10
11
12
13
14
webs. Ecol. Lett. 3, 131–136. (doi:10.1046/j.1461-0248.
2000.00130.x)
Montoya, J. M., Pimm, S. L. & Sole, R. V. 2006 Ecological networks and their fragility. Nature 442, 259–264.
(doi:10.1038/nature04927)
Paine, R. T. 1966 Food web complexity and species
diversity. Am. Nat. 100, 65–75. (doi:10.1086/282400)
Ives, A. R. & Cardinale, B. J. 2004 Food-web interactions
govern the resistance of communities after non-random
extinctions. Nature 429, 174–177. (doi:10.1038/
nature02515)
Brose, U. 2011 Extinctions in complex, size-structured
communities. Basic Appl. Ecol. 12, 557 –561. (doi:10.
1016/j.baae.2011.09.010)
Ebenman, B. 2011 Response of ecosystems to realistic
extinction sequences. J. Anim. Ecol. 80, 307 –309.
(doi:10.1111/j.1365-2656.2011.01805.x)
de Visser, S. N., Freymann, B. P. & Olff, H. 2011 The
Serengeti food web: empirical quantification and analysis
of topological changes under increasing human impact.
J. Anim. Ecol. 80, 484 –494. (doi:10.1111/j.1365-2656.
2010.01787.x)
Eklof, A. & Ebenman, B. 2006 Species loss and secondary extinctions in simple and complex model
communities. J. Anim. Ecol. 75, 239 –246. (doi:10.
1111/j.1365-2656.2006.01041.x)
Petchey, O. L., Eklof, A., Borrvall, C. & Ebenman, B.
2008 Trophically unique species are vulnerable to cascading extinction. Am. Nat. 171, 568–579. (doi:10.
1086/587068)
Curtsdotter, A., Binzer, A., Brose, U., de Castro, F.,
Ebenman, B., Eklöf, A., Riede, J. O., Thierry, A. &
Rall, B. C. 2011 Robustness to secondary extinctions:
comparing trait-based sequential deletions in static and
dynamic food webs. Basic Appl. Ecol. 12, 571–580.
(doi:10.1016/j.baae.2011.09.008)
Bukovinszky, T., van Veen, F. J. F., Jongema, Y. & Dicke,
M. 2008 Direct and indirect effects of resource quality on
food web structure. Science 319, 804– 807. (doi:10.1126/
science.1148310)
Abrams, P. A. & Nakajima, M. 2007 Does competition
between resources change the competition between
their consumers to mutualism? Variations on two
themes by Vandermeer. Am. Nat. 170, 744–757.
(doi:10.1086/522056)
Dethier, M. N. & Duggins, D. O. 1984 An indirect commensalism between marine herbivores and the
Biol. Lett. (2012)
15
16
17
18
19
20
21
22
23
24
25
26
27
963
importance of competitive hierarchies. Am. Nat. 124,
205 –219. (doi:10.1086/284264)
Dodson, S. I. 1970 Complementary feeding niches sustained by size-selective predation. Limnol. Oceanogr. 15,
131 –137.
Vandermeer, J. 1980 Indirect mutualism: variations on a
theme by Levine. Am. Nat. 116, 441–448. (doi:10.1086/
283637)
Levine, S. H. 1976 Competitive interactions in ecosystems. Am. Nat. 110, 903 –910. (doi:10.1086/283116)
Davidson, D. W., Inouye, R. S. & Brown, J. H. 1984
Granivory in a desert ecosystem: experimental evidence
for indirect facilitation of ants by rodents. Ecology 65,
1780– 1786. (doi:10.2307/1937774)
Brown, J. H. & Davidson, D. W. 1986 Do desert rodent
populations increase when ants are removed reply.
Ecology 67, 1423–1425. (doi:10.2307/1938698)
Galindo, C. 1986 Do desert rodent populations increase
when ants are removed. Ecology 67, 1422 –1423. (doi:10.
2307/1938697)
van Veen, F. J. F., Morris, R. J. & Godfray, H. C. J. 2006
Apparent competition, quantitative food webs, and the
structure of phytophagous insect communities. Ann.
Rev. Entomol. 51, 187 –208. (doi:10.1146/annurev.ento.
51.110104.151120)
Harmon, J. P., Moran, N. A. & Ives, A. R. 2009 Species
response to environmental change: impacts of food web
interactions and evolution. Science 323, 1347 –1350.
(doi:10.1126/science.1167396)
Morris, R. J., Lewis, O. T. & Godfray, H. C. J. 2004
Experimental evidence for apparent competition in a tropical forest food web. Nature 428, 310– 313. (doi:10.
1038/nature02394)
van Veen, F. J. F., van Holland, P. D. & Godfray, H. C. J.
2005 Stable coexistence in insect communities due to
density- and trait-mediated indirect effects. Ecology 86,
3182– 3189. (doi:10.1890/04-1590)
R Development Core Team. 2009 R: a language and
environment for statistical computing. Vienna, Austria:
R foundation for statistical computing.
Lawton, J. H. & Hassell, M. P. 1981 Asymmetrical competition in insects. Nature 289, 793– 795. (doi:10.1038/
289793a0)
Ebenman, B. & Jonsson, T. 2005 Using community viability analysis to identify fragile systems and keystone
species. Trends Ecol. Evol. 20, 568 –575. (doi:10.1016/j.
tree.2005.06.011)