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Journal Article•DOI•

Long‐term responses of zooplankton to invasion by a planktivorous fish in a subarctic watercourse

Per-Arne Amundsen1, Anna Siwertsson1, Raul Primicerio1, Thomas Bøhn1•
Norwegian College of Fishery Science1
01 Jan 2009-Freshwater Biology (Wiley)-Vol. 54, Iss: 1, pp 24-34
TL;DR: Increased predation pressure following the vendace invasion induced many effects on the crustacean zooplankton, and this paper documents comprehensive and strong direct and indirect long-term impacts of an introduced non-native predator on the native prey community.
Abstract: 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, specialized 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-year 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.

Summary (2 min read)

Jump to: [INTRODUCTION] – [METHODS] – [RESULTS] – [DISCUSSION] and [Legends to figures:]

INTRODUCTION

  • Of alien species represents one of the greatest threats to global biodiversity (Gido & Brown, 1999; Davis, 2003).
  • 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.
  • 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).
  • Accordingly, in several cladoceran species a smaller size at first reproduction has been demonstrated to occur with increasing predation pressure from fish (Stibor, 1992; Vonder Brink & Vanni, 1993; Weber & Declerck, 1997).

METHODS

  • The Pasvik water system (69oN, 29oE) originates from Lake Inari (1102 km2) in Finland, runs into Russia and then defines the border between Norway and Russia for a length of about 120 km.
  • The lake is dimictic, oligotrophic and humic with a Secchi-depth from 2-4 m.
  • From each sampling occasion, the body size of Daphnia spp. was measured under a binocular microscope with 40 X magnification on 50 females and, when possible, on up to 40 females with subitaneous eggs.
  • Binary logistic regressions were performed with the number of eggs (one or two) as the dependent variable, and body length and year as independent variables.

RESULTS

  • The total density of crustacean zooplankton showed a strong negative trend during the study period, including a sharp decrease from 1991 to 1993, followed by a recovery in abundance in 1995, and thereafter a steep decline towards 2002 (Fig. 2a).
  • Excluding this species from the analyses gave a significant overall decline in the total density of other zooplankton species over the time period from 1991 to 2002 (Linear regression; P<0.05, R2=0.44).
  • The most abundant cladocerans were Bosmina longirostris, Bosmina longispina and Daphnia cristata, whereas Daphnia longiremis, Daphnia longispina (O.F.M), Ceriodaphnia quadrangula (O.F.M), Holopedium gibberum Zaddach and Leptodora kindtii occurred more occasionally.
  • The size at first reproduction decreased significantly over the study period for the two Bosmina species (Fig. 5; Table 2; logistic regression: P<0.001 for both species), with the largest decrease being observed in B. longispina.
  • The size at first reproduction also decreased significantly in Daphnia spp. during the study, but with a less clear-cut trend than for the Bosmina species (Table 2; logistic regression: P<0.05).

DISCUSSION

  • Throughout the whole study, the zooplankton community in Ruskebukta was dominated by small cladocerans, in particular D. cristata, B. longispina and B. longirostris.
  • The present findings confirm that efficient and selective predation by vendace may have very strong effects on the density and composition of the zooplankton community, and also demonstrate the impact of an invading predator on its prey community.
  • The size at first reproduction also decreased during the study period in all the examined cladoceran species, and B. longispina seemed to be the most affected.
  • Whatever the actual mechanisms are in the present system, the observed decreases in size at first reproduction demonstrate severe impacts of the alien predator even on life history traits of the prey populations.
  • The authors also acknowledge two anonymous referees for their helpful comments and suggestions.

Legends to figures:

  • Relative contribution of vendace in gillnet catches from the pelagic fish community in Ruskebukta during the time period from 1991 to 2002.
  • Stippled line represents asymptotic power curve fitted to the data.
  • Fig. 2. Total density (a), species diversity (b) and relative species composition (c) of the crustacean zooplankton community in Ruskebukta during the study period.
  • For equations and statistics of regression lines, see Table 1. Fig.
  • Size at first reproduction (body length with 50% egg-bearing females, EL50) of B. longispina and B. longirostris during the study period.

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Figures (3)

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1
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
2
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.
3
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
4
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;
5
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
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Abstract: The Lake Victoria fish fauna included an endemic cichlid flock of more than 300 species. To boost fisheries, Nile perch (Lates sp.) was introduced into the lake in the 1950s. In the early 1980s an explosive increase of this predator was observed. Simultaneously, catches of haplochromines decreased. This paper describes the species composition of haplochromines in a research area in the Mwanza Gulf of Lake Victoria prior to the Nile perch upsurge. The decline of the haplochromines as a group and the decline of the number of species in various habitats in the Mwanza Gulf was monitored between 1979 and 1990. Of the 123+ species originally caught at a series of sampling stations ca. 80 had disappeared from the catches after 1986. In deepwater regions and in sub-littoral regions haplochromine catches decreased to virtually zero after the Nile perch boom. Haplochromines were still caught in the littoral regions where Nile perch densities were lower. However, a considerable decrease of species occurred in these regions too. It is expected that a remnant of the original haplochromine fauna will survive in the littoral region of the lake. Extrapolation of the data of the Mwanza Gulf to the entire lake would imply that approximately 200 of the 300+ endemic haplochromine species have already disappeared, or are threatened with extinction. Although fishing had an impact on the haplochromine stocks, the main cause of their decline was predation by Nile perch. The speed of decline differed between species and appeared to depend on their abundance and size, and on the degree of habitat overlap with Nile perch. Since the Nile perch upsurge, the food web of Lake Victoria has changed considerably and the total yield of the fishery has increased three to four times. Dramatic declines of native species have also been observed in other lakes as a result of the introduction of alien predators. However, such data concern less speciose communities and, in most cases, the actual process of extinction has not been monitored.

454 citations

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Boris Worm1, Heike K. Lotze2, Heike K. Lotze1, Helmut Hillebrand3, Ulrich Sommer2 •
Dalhousie University1, University of Kiel2, Uppsala University3
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TL;DR: The effects of consumers and nutrients on diversity consistently depend on each other, and that the direction of their effects and peak diversity shift between sites of low and high productivity, suggesting human impacts on nutrient supply and food-web structure have strong and interdependent effects on species diversity and ecosystem functioning, and must therefore be managed together.
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453 citations

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Jonathan Cox1, Steven L. Lima1•
Indiana State University1
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443 citations

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Predation, Body Size, and Composition of Plankton

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01 Mar 2008-Biological Invasions
Thomas Bøhn, Per-Arne Amundsen, Ashley D. Sparrow
Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times

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01 Nov 2006-Molecular Ecology
Kjartan Østbye, Per-Arne Amundsen, Louis Bernatchez, Anders Klemetsen, Rune Knudsen, Roar Kristoffersen, T. F. Næsje, Kjetil Hindar 
Sympatric diversification as influenced by ecological opportunity and historical contingency in a young species lineage of whitefish

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01 Jan 2010-Evolutionary Ecology Research
Anna Siwertsson, Rune Knudsen, Kimmo K. Kahilainen, Kim Præbel, Raul Primicerio, Per-Arne Amundsen 
Frequently Asked Questions (1)
Q1. What are the contributions in "Long-term responses of zooplankton to invasion by a planktivorous fish in a subarctic watercourse" ?

Strayer et al. this paper studied the long-term effects of predation on the planktonic prey community over a 12-yr period during the establishment of a specialised zooplanktivore.