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Long-term responses of zooplankton to invasion by a
planktivorous fish in a subarctic watercourse
Per-Arne Amundsen*, Anna Siwertsson*, Raul Primicerio* & Thomas Bøhn*
§
* Department of Aquatic Biosciences, Norwegian College of Fishery Science, University of
Tromsø, Tromsø, Norway
§
Norwegian Institute of Gene Ecology, Breivika, Tromsø, Norway
Correspondence: Per-Arne Amundsen, Norwegian College of Fishery Science, University of
Tromsø, N-9037 Tromsø, Norway.
E-mail: Per-Arne.Amundsen@nfh.uit.no
Keywords: invasion, zooplankton, planktivory, Daphnia, Bosmina, predation
Published in Freshwater Biology (2009) 54, 24–34. doi: 10.1111/j.1365-
2427.2008.02088.x
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Summary
1. Introduced or invading predators may have strong impacts on prey populations of the
recipient community mediated by direct and indirect interactions. The long-term progression
of predation effects, covering the invasion and establishment phase of alien predators,
however, has rarely been documented.
2. This paper documents the impact of an invasive, specialised planktivorous fish on its prey
in a subarctic watercourse. Potential predation effects on the crustacean plankton, at the
community, population and individual levels, were explored in a long-term study following
the invasion by vendace (Coregonus albula).
3. Over the 12-yr period, the density and species richness of zooplankton decreased, smaller
species became more abundant, and Daphnia longispina, one of the largest cladocerans, was
eliminated from the zooplankton community.
4. Within the dominant cladocerans, including Daphnia spp., Bosmina longispina and
Bosmina longirostris, the body size of ovigerous females and the size at first reproduction
decreased after the arrival of the new predator. The clutch sizes of Daphnia spp. and B.
longirostris also increased.
5. Increased predation pressure following the vendace invasion induced many effects on the
crustacean zooplankton, and we document comprehensive and strong direct and indirect long-
term impacts of an introduced non-native predator on the native prey community.
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INTRODUCTION
The introduction of alien species represents one of the greatest threats to global biodiversity
(Gido & Brown, 1999; Davis, 2003). Introduced predators may have a particularly strong
impact on recipient communities due to a high vulnerability of naïve prey to new predators
(Park, 2004). Prey naiveté is most common in freshwater ecosystems (Cox & Lima, 2006),
and isolated environments like lakes and islands are particularly sensitive to predator
introductions (Kaufman, 1992; Courchamp et al., 2003). In lakes, invasive predators may
even be able to drive native species to extinction (Zaret & Paine, 1973; Witte et al., 1992).
Classic examples of strong predatory impacts include lacustrine introductions of
planktivorous fish that have caused extinction of large-sized zooplankton species (Hrbáček et
al., 1961; Brooks & Dodson, 1965).
Most studies of predation effects on zooplankton are short-term comparisons of the prey
communities before and after predator introductions, or comparisons of similar systems with
and without the predator (Hrbáček et al., 1961; Brooks & Dodson, 1965; Hall et al., 1976;
DeMelo, France & McQueen, 1992). Such short-term surveys may lack the power to separate
weak trends from natural variations (Elliott, 1994). Furthermore, such snapshot studies can
not distinguish between direct and indirect effects of predator introductions, and do not
provide any information on the transitory dynamics between different prey community states.
Thus, based on short-term studies, it is not possible to conclude which mechanisms drive the
changes in the prey community or to quantify the rates of change, precluding in-depth
understanding and predictions. Long-term studies of predator impact on prey are necessary to
obtain information on relevant mechanisms and transient dynamics, but have rarely been
performed (Strayer et al., 2006). The present contribution relates to the introduction and
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invasion of an alien fish species, the vendace Coregonus albula (Linnaeus, 1758), in a
subarctic watercourse, examining the long-term effects on the planktonic prey community
over a 12-yr period during the establishment of this specialised zooplanktivore.
Predation by planktivorous fish has large impacts on the dynamics and structure of
zooplankton communities (Zaret, 1980; Lazzaro, 1987; Gliwicz & Pijanowska, 1989). The
primary, direct effect is an increased mortality rate of the prey. However, predation is often
highly selective and most planktivorous fish are visual predators that select the largest visible
prey (O'Brien, 1987; Gliwicz & Pijanowska, 1989; Lampert & Sommer, 1997). Cladocerans
are often preferred prey since they have a conspicuous pattern of motion (Zaret, 1980) and are
easy to capture compared to copepods which have a more effective escape response (O'Brien,
1987; Lampert & Sommer, 1997). The egg clutches carried by gravid cladocerans may further
increase their vulnerability, and selection of ovigerous females and females carrying a large
number of eggs may strengthen the predation effects on prey density, composition and
demography (Gliwicz, 1981; Dawidowicz & Gliwicz, 1983).
In addition to the numerical, direct effects of predation, prey populations may be affected by
invasive predators via trait-mediated interactions (Bolker et al., 2003). Several cladoceran
species are able to adjust their life-history in response to increased predation risk detected via
chemical cues associated with digested prey (Stabell, Ogbebo & Primicerio, 2003; Pohnert,
Steinke & Tollrian, 2007). Cues associated with predation risk from fish are known to
anticipate the onset of reproduction in order to increase the chance of reproducing
successfully before being eaten (Taylor & Gabriel, 1992; Larsson & Dodson, 1993; Lass &
Spaak, 2003). Accordingly, in several cladoceran species a smaller size at first reproduction
has been demonstrated to occur with increasing predation pressure from fish (Stibor, 1992;
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Vonder Brink & Vanni, 1993; Weber & Declerck, 1997). Clutch size has also been found to
increase when predation from fish intensifies (Dodson, 1989; Stibor, 1992; Vonder Brink &
Vanni, 1993). Hence, increased predation from planktivorous fish may result in a multitude of
effects, mediated by direct and indirect interactions, including a decrease in zooplankton
abundance (Gliwicz, 1981; Hamrin & Persson, 1986; Persson et al., 2004), changes in
community and population structure towards smaller species and smaller individuals within
the species (Brooks & Dodson, 1965; Hall, Cooper & Werner, 1970), life-history
modifications (Stibor, 1992; Weider & Pijanowska, 1993) and morphological adaptations
(Dodson, 1988, 1989; Kolar & Wahl, 1998).
Few studies have addressed the impacts of zooplanktivore fish in subarctic and arctic systems
and, to our knowledge, long-term studies of the impact of invasions in the subarctic are absent.
These systems are presently undergoing changes associated with climate warming that are
expected to favour the successful invasion of specialist planktivores (Primicerio et al., 2007).
It is therefore important to document and understand the long-term implications of such
invasions. In the subarctic Pasvik water system, northern Norway, the opportunity to study
long-term ecological responses during the establishment of an alien predator arose when
vendace invaded the watercourse in the late 1980’s (Amundsen et al., 1999). The vendace is a
highly specialised zooplanktivore (e.g., Svärdson, 1976; Hamrin, 1983; Bøhn & Amundsen,
1998) and established successfully as the dominant pelagic fish species during the 1990’s
(Amundsen et al., 1999; Bøhn et al., 2004). Whitefish (Coregonus lavaretus (Linnaeus, 1758))
dominated the native limnetic fish community, but has been displaced from the pelagic habitat
due to competitive interactions with vendace (Amundsen et al., 1999; Bøhn & Amundsen,
2001, Bøhn et al., 2008). The vendace thus represents a new and highly efficient predator of
the native crustacean plankton. The trends in the zooplankton community following the