Multispecies interactions among a plant parasite, a
pollinator and a seed predator affect the reproductive
output of an invasive plant, Cytisus scoparius
JANE N. PRIDER,* JOSÉ M. FACELLIAND JENNIFER R. WATLING
Ecology and Evolutionary Biology, School of Earth and Environmental Sciences,The University of
Adelaide, Adelaide, South Australia, Australia
Abstract Interactions between species pairs are almost always mediated by interactions with other species. The
outcomes of these multispecies interactions are often difficult to predict and are rarely studied. In addition to their
theoretical importance, multispecies interactions are also important for management situations. Where multiple
agents are used to control invasive species, interactions between agents may either enhance or reduce the impacts
on the target species, or may simply have additive effects. In this study, conducted in a Mediterranean-type
woodland in Australia, we examined how the interaction between an invasive legume, Cytisus scoparius (Legumi-
nosae), its pollinator, Apis mellifera and a seed predator, Bruchidius villosus (Bruchidae), are modified by a native
hemiparasitic vine, Cassytha pubescens (Loranthaceae). The parasite had a direct negative effect on C. scoparius,
reducing flowering by 50% and consequently fruit and seed production. Despite having fewer flowers, infected
plants had the same proportion of ‘tripped’ flowers, an indirect measure of pollinator visitation, as uninfected
plants; although fruit formed on infected plants it was more likely to abort prematurely. Seed predation by B. villosus
was lower on parasite-infected C. scoparius plants than in uninfected plants. Although Ca. pubescens had an
antagonistic effect on B. villosus, in consort, the two agents reduced overall seed production by an average of 62%.
The acquired parasite Ca. pubescens was more effective in reducing reproductive output than the introduced seed
predator, B. villosus, and shows potential as a biocontrol agent for C. scoparius.We documented a subadditive effect
of two biological enemies on the invasive species, where the acquired parasite had a stronger effect than the
introduced seed predator.
Key words: Bruchidius villosus, Cassytha pubescens, enemy release, Scotch broom, tripartite interaction.
INTRODUCTION
Because of the biological complexity inherent in eco-
logical communities, most studies of species interac-
tions have focussed on direct pairwise relationships;
however, organisms typically interact simultaneously
with a number of mutualists and antagonists. The inci-
dence or intensity of pairwise interactions between
species can be altered by the presence of other organ-
isms, resulting in indirect interactions that can have
synergistic or non-additive effects on plant fitness
(Wootton 1993; Herrera 2000; Bronstein et al. 2003;
Strauss & Irwin 2004; Mitchell et al. 2006; Brody et al.
2008). Where species introductions occur, new inter-
actions will be established that will impact on both the
invading species and the host community. Thus, the
ability of an introduced plant to invade a community
depends on the network of interactions it establishes
with other organisms, both native and introduced, in
the new range. These networks include negative inter-
actions such as competition, herbivory and parasitism,
as well as positive interactions such as mutualistic sym-
bioses and pollination (Richardson et al. 2000; Shea &
Chesson 2002; Noonburg & Byers 2005; Eppstein &
Molofsky 2007). It has been proposed that escaping
from natural enemies in the original system also con-
tributes to success in the invaded system (Maron &
Vila 2001; Keane & Crawley 2002; Parker & Hay
2005). Conversely, species may have evolved tolerance
to their native enemies (Callaway & Aschehoug 2000;
Bergelson et al. 2001), but may be more susceptible to
novel enemies encountered in the invaded system
(Maron & Vila 2001; Parker et al. 2006; Verhoeven
et al. 2009).
Reproductive traits of introduced species are im-
portant determinants of their successful spread and
eventual dominance in a new range (Rejmánek &
Richardson 1996). Biotic interactions that constrain
reproductive output can have important effects on the
success of invasive species when there is a link between
seed production and population size (Turnbull et al.
*Corresponding author. Present address: Department of
Water, Land and Biodiversity Conservation, PO Box 2834, Ade-
laide, SA 5001, Australia. (Email: jane.prider@sa.gov.au)
Accepted for publication March 2010.
Austral Ecology (2011) 36, 167–175
© 2010 The Authors doi:10.1111/j.1442-9993.2010.02132.x
Journal compilation © 2010 Ecological Society of Australia