Interactions between invading benthivorous fish and native whitefish in subarctic lakes

Interactions between invading benthivorous fish and nativewhitefish in subarctic lakes

BRIAN HAYDEN* ,† , TI INA HOLOPAINEN‡, PER-ARNE AMUNDSEN§, ANTTI P. ELORANTA¶, RUNE

KNUDSEN§, KIM PRÆBEL§ , 1 AND KIMMO K. KAHILAINEN*,†

*Kilpisj€arvi Biological Station, University of Helsinki, Kilpisj€arvi, Finland†Department of Environmental Sciences, University of Helsinki, Helsinki, Finland‡Department of Biology, Faculty of Science and Forestry, University of Eastern Finland, Joensuu, Finland§Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, Tromsø, Norway¶Department of Biological and Environmental Sciences, University of Jyv€askyl€a, Jyv€askyl€a, Finland

SUMMARY

1. Many species are expanding their distribution towards higher latitudes and altitudes in response

to climate change. These range shifts are expected to change fish community structure and alter

food-web dynamics in subarctic lakes. However, the impacts of invading species on native fish and

invertebrate prey communities remain understudied.

2. The trophic ecology of invasive species determines the likelihood of direct resource competition

with native taxa. In Northern Europe, perch (Perca fluviatilis), a trophic generalist, and ruffe (Gymno-

cephalus cernuus), a benthic specialist, are expanding their distribution ranges northwards, colonising

lakes inhabited by a native generalist, whitefish (Coregonus lavaretus). We predicted that increased

fish diversity and density would deplete the invertebrate community and increase resource competi-

tion between native and invasive species.

3. To assess the degree of resource competition between native and invasive species, we compared

(i) fish and invertebrate community structure; (ii) diet and stable carbon and nitrogen ratios of white-

fish, ruffe and perch and (iii) growth, condition and relative population size of whitefish in two non-

invaded lakes with two lakes containing one and two lakes containing both invasive species. Each

lake was sampled on a single occasion between August and September.

4. Benthic macroinvertebrate density and community structure were unaffected by increased con-

sumer diversity, while top-down control of pelagic zooplankton density and size was evident in

lakes with increased fish diversity.

5. Differences in diet and stable isotope ratios were evident between all whitefish populations,

although these were not directly related to the presence of invasive species. Specialised adaptations

of invasive species may confer a competitive advantage in invaded lakes; ruffe dominated the pro-

fundal niche, while perch displayed an ontogenetic shift to piscivory, reducing niche overlap with

native whitefish.

6. Growth rate and population density of whitefish were largely independent of fish community

structure and were governed by local variations in lake productivity. However, there was a sign of

lowered condition of whitefish in invaded systems. Shallow and more productive lakes with higher

food availability supported populations of native and invasive species.

7. Our findings indicate that trophic specialisations of invasive species play a key role in determining

their impacts on the systems they invade. This study focussed on early stages of invasion, and the

outcome of species interactions may change following the establishment of new species. In addition,

these impacts will not be uniform across the invaded landscape as lake-specific variations in

Correspondence: Brian Hayden, Department of Environmental Sciences, University of Helsinki, P.O. Box 65, FI-00014, Finland.

E-mail: [email protected] Present address: Kim Præbel, Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, P.O.

Box 1066, Blindern, N-0315, Oslo, Norway.

1234 © 2013 Blackwell Publishing Ltd

Freshwater Biology (2013) 58, 1234–1250 doi:10.1111/fwb.12123

morphometry and resource availability will alter the competitive balance between native and inva-

sive species.

Keywords: climate change, competition, fish, food webs, invasive species, invertebrates, lakes, stable iso-topes

Introduction

Shifts in distribution driven by climate change have

been recorded in numerous terrestrial, marine and fresh-

water species (Mack et al., 2000; Graham & Harrod,

2009; Jeppesen et al., 2012). Such range shifts may lead

to novel species assemblages (Pereira et al., 2010; Comte

et al., 2013) and altered food-web structures (Vander

Zanden, Casselman & Rasmussen, 1999; Simon & Town-

send, 2003), which can have detrimental effects on

native species and ecosystem functioning (Parmesan,

2006). Investigations of trophic interactions between

native and invasive species at their current distribution

range boundaries can provide an insight into the likely

repercussions of range expansion.

Bioclimate envelope models (i.e. direct extrapolation

of species range with changing temperature) are helpful

to detail how species distributions may change in accor-

dance with increasing ambient temperature (Pearson &

Dawson, 2003). As fish can be classified into ‘warm’,

‘cool’ and ‘cold water’ thermal guilds, depending on

their preferred temperature range (Fry, 1971; Magnuson,

Crowder & Medvick, 1979), they make ideal candidates

for bioclimatic modelling. However, such models

exclude the interspecific ecological interactions that

determine species distributions at a local level (Hampe,

2004). Here, ecological interactions (i.e. predation and

resource competition) with native species determine not

only the degree to which invading species will succeed

in novel environments, but also the impacts of invasions

upon the receiving ecosystem (Bystr€om et al., 2007;

Vitule, Freire & Simberloff, 2009). The ecological strate-

gies of native and invasive species are important in this

regard (Marchetti, Moyle & Levine, 2004; Sax et al.,

2007). For example, an introduced specialist may be able

to dominate its preferred resource and exclude native

competitors (Bøhn & Amundsen, 2001; Bøhn, Amundsen

& Sparrow, 2008). Conversely, an invasive generalist

may be able to utilise a variety of resources in the novel

habitat to alleviate direct competition with native taxa.

In addition to competitive interactions, the carrying

capacity of the system is crucial in determining whether

additional species will be able to establish and have a

deleterious effect upon the receiving ecosystem (Lock-

wood, Hoopes & Marchetti, 2007). When the system

approaches carrying capacity, consumers will exhibit a

controlling effect on the abundance of prey items, and

consequently, instances of resource competition between

native and invasive species will increase (Bøhn &

Amundsen, 2001). In addition, climate-driven range

shifts are not limited to one species, as multiple species

will be likely to migrate into new habitats during a simi-

lar timeframe (Graham & Harrod, 2009). This poses

questions regarding the impacts, not only of increased

consumer numbers, but also novel assemblages of spe-

cies and foraging strategies which affect both resident

prey and fish communities.

Subarctic lakes provide ideal ecosystems to study these

questions as they maintain relatively simple food webs.

The dominant native fish species in subarctic Fennoscan-

dian lakes is the monomorphic large sparsely rakered

(LSR) whitefish (Coregonus lavaretus), which is an ecologi-

cal generalist utilising both pelagic and benthic prey

(Kahilainen et al., 2007; Harrod, Mallela & Kahilainen,

2010). In some large and deep lakes, whitefish have

undergone adaptive radiations into specialist pelagic and

benthic morphs, but most lakes are inhabited by mono-

morphic LSR whitefish (Østbye et al., 2006; Siwertsson

et al., 2010; Kahilainen et al., 2011). This region represents

the northern range limit for percid species; perch

(Perca fluviatilis) and ruffe (Gymnocephalus cernuus)

(Tammi et al., 2003), both of which have potential to

expand their range northwards in parallel with increas-

ing ambient water temperatures. Perch is an ecological

generalist utilising ontogenetic dietary shifts from zoo-

plankton to benthic macroinvertebrates before finally

becoming piscivorous (Persson, 1983; Amundsen et al.,

2003). Ruffe is a benthic specialist with a diet dominated

by chironomid larvae and a special preference for egg

predation (Ogle, 1998). Invasive populations of ruffe have

been recorded outside the native range of the species

(Winfield, Dodge & R€osch, 1998). As an efficient benthi-

vore, ruffe is able to dominate benthic resources and

potentially to cause detrimental trophic shifts in native

species, particularly generalists such as perch and white-

fish (Bergman & Greenberg, 1994; Adams & Maitland,

1998). Range expansion by ruffe and perch into lakes

containing resident whitefish provides an opportunity to

examine the ecological processes of early stage invasion

in fish communities (Lockwood et al., 2007).

© 2013 Blackwell Publishing Ltd, Freshwater Biology, 58, 1234–1250

Benthivorous fish invasions in subarctic lakes 1235

We investigated the trophic ecology of native white-

fish in non-invaded (NI) lakes and in lakes containing

one or both invasive percids, highlighting the effects of

increased consumer diversity on invertebrate community

structure and in turn on growth, condition, length and

population size of native whitefish. We tested three prin-

cipal hypotheses: first, that increased fish diversity and

density would alter the community structure of benthic

macroinvertebrates and zooplankton towards smaller

species and body sizes via selective predation (Brooks &

Dodson, 1965; Blumenshine, Lodge & Hodgson, 2000;

Amundsen et al., 2009); second, that perch and ruffe, as

more efficient benthivores (Ogle, 1998; Amundsen et al.,

2003), would dominate the benthic prey resources result-

ing in a dietary shift towards pelagic feeding by general-

ist whitefish; third, that whitefish would exhibit reduced

levels of somatic growth and condition in invaded sys-

tems due to resource competition with the invasive spe-

cies (Bøhn & Amundsen, 2004).

Methods

The study was conducted on six lakes in north-western

Fennoscandia (Fig. 1), comprising two replicates of (i)

whitefish-dominated NI lakes; (ii) lakes containing

whitefish and ruffe (WR) and (iii) lakes containing

whitefish, ruffe and perch (WRP). Numbers of fish spe-

cies in each lake varied from 4 to 12, of which the core-

gonids [LSR whitefish, densely rakered (DR) whitefish

and vendace Coregonus albula] and invasive percids

(ruffe and perch) were the most abundant (Table 1).

Additional fish species, most notably brown trout (Salmo

trutta), grayling (Thymallus thymallus), pike (Esox lucius)

and burbot (Lota lota), were present in some lakes

(Table 1). Sampling was conducted on one occasion

between August and September 2011, except in Lake

Palo, which was sampled in August 2009. With the

exception of Lake Palo, which is classed as mesotrophic,

all lakes were oligotrophic as is typical of this region

(Table 1).

Field sampling

Bathymetric maps were created for each lake using

hydroacoustics. Vertical light profiles were measured

so that compensation depths (depth at which

light = 1% of surface light) could be calculated (Lam-

pert & Sommer, 2007). Littoral (benthic areas situated

in waters shallower than the compensation depth),

profundal (benthic areas deeper than compensation

depth) and pelagic (open water above the profundal)

zones were subsequently identified and quantified in

each lake prior to sampling.

Benthic macroinvertebrates were collected from a tran-

sect using an Ekman grab (sampling area of 234 cm2)

following a previously established methodology (Kahilai-

nen, Lehtonen & K€on€onen, 2003). Lake Palo was sampled

using a larger Ekman grab (sampling area of 272 cm2).

Three replicates at each depth were taken along a depth

contour transect at depths of 1, 2, 3, 5, 10, 15 and 20 m

(when lake depth permitted) to represent a continuum

from littoral to profundal habitats. Samples were sieved

through a 0.5-mm mesh, and individuals were subse-

quently identified to family level and macroinvertebrate

density (individuals m�2) calculated for each depth. Blot-

ted mass (g) of each group was weighed (accuracy

0.0001 g), and biomass values (g m�2) were calculated for

littoral and profundal macroinvertebrate communities in

each lake. Mean individual mass was obtained by divid-

ing total invertebrate biomass by the number of individu-

als. Biomass data were not available for Lake Palo due to a

restricted sampling procedure in place at that time (2009).

Pelagic zooplankton were sampled using a zooplank-

ton net (25 cm diameter, 50-lm mesh size) hauled verti-

cally through the entire water column. Individuals were

identified to family level, and zooplankton density (indi-

viduals L�1) was determined for each lake. Body length

(accuracy of 0.01 mm) of a random subsample (n = 30,

when available) of individuals of each family was mea-

sured using an Olympus CK30-F200 microscope (Olym-

pus Optical Co., Postfach Hamburg, Germany). Body

length of all small benthic crustaceans (i.e. Ostracoda,

Eurycercus spp. and Megacyclops spp.) sampled was

recorded in each lake except Lake Palo.

Fish were sampled using gill nets. Selection bias associ-

ated with gill netting is well established (Carol & Garc�ıa-

Berthou, 2007); however, the methodology remains the

most effective and widely employed way of sampling fish

in lakes (CEN, 2005). To overcome the inherent bias, a

wide selection of mesh sizes were used and sampling

effort was standardised between systems. Gill net series

consisting of eight nets, each 30 9 1.8 m with knot-to-

knot mesh sizes of 12, 15, 20, 25, 30, 35, 45 and 60 mm

(Kahilainen et al., 2004), and a 30 9 1.5 m Nordic multi-

mesh net, which was comprised of 12 equidistant 2.5 m

panels with mesh sizes ranging from 5 to 55 mm (Appel-

berg, 2000). Nets were set overnight in littoral, profundal

and pelagic zones of each lake. The number of nets set

was determined by the size of the lake, but at least three

replicates were conducted in each habitat type (littoral,

profundal and pelagic). The shallow littoral nature of

Lakes Kolta and Palo precluded pelagic/profundal sam-


1236 B. Hayden et al.

pling. Consequently, fish density analysis was limited to

data collected from benthic (combined littoral and pro-

fundal) gill nets, which were comparable across all sys-

tems. Density and biomass catch per unit effort (CPUE)

values were calculated as number of fish and grams of

fish per gill net series per hour.

All fish captured were identified to species level in

the field and whitefish were identified to morph accord-

ing to head and gill raker morphology (Kahilainen et al.,

2011). Total length (�1 mm) and blotted mass (�0.1 g)

were recorded for each individual, and representative

subsamples of fish were frozen (�20 °C) for subsequent

69°

70°

71°

68°Latit

ude

(°N

)

16° 28°20° 24°

(a)

FinlandSweden

Norway

Russia

L. Kuohkima (NI)

L. Kolta (NI)

L. Oiko(WR)

L. Kivi(WRP)

L. Ropi(WR)

L.Palo(WRP)

(b)

20° 23°21° 22°

68°

68.5°

69°

Longitude (°E)19°

(b)

Fig. 1 Location of study lakes in the (a) north–western Fennoscandia and (b) the upper reaches of the Tornio–Muoniojoki catchment.

Table 1 Biotic and abiotic characteristics of the non-invaded (NI), whitefish and ruffe (WR), and whitefish, ruffe and perch (WRP) lakes

Parameter L. Kolta L. Kuohkima L. Oiko L. Ropi L. Kivi L. Palo

Lake type NI NI WR WR WRP WRP

Latitude (°N) 69°03′ 69°03′ 68°50′ 68°41′ 68°49′ 68°34′Longitude (°E) 20°30′ 20°33′ 21°13′ 21°35′ 21°15′ 23°21′Surface area (km2) 1.3 0.3 1.2 1.3 3.5 3.5

Altitude (m a.s.l.) 490 488 448 398 445 346

Max depth (m) 3 10 10 20 10 2

Mean depth (m) 1.1 2.6 3.1 6.9 2.8 0.8

Secchi depth (m) 3 4.5 2.5 2.5 3 2

Compensation depth (m) >3 8 5 5 5 >2Total P (lg L�1) – – 7* 10* 7* 21†

Total N (lg l�1) – – 215* 273* 201* 470†

Species composition a, b, c, d a, b, c, d, e, f a, b, c, d, e, g, h a, b, c, d, e, f, g,

h, i, j, k, l

a, b, c, e, g, i, l a, b, c, f, g, h,

i, l, m

LSR whitefish density 2.1 (1.1) 4.4 (1.7) 8.6 (4.3) 1.1 (1.2) 9.5 (4.6) 0.6 (0.4)

LSR whitefish biomass 322 (282) 677 (152) 280 (101) 91 (99) 316 (154) 372 (224)

Ruffe biomass – – 23 (6) 8 (3) 34 (32) 50 (44)

Perch biomass – – – – 3089 (4985) 43 (37)

Pike biomass 82 (89) 74 (48) 93 (100) 64 (112) 135 (177) 67 (65)

Vendace biomass – – – – – 42 (28)

DR whitefish biomass – – – 198 (134) – –Other species biomass 1 (1) 15 (18) 10 (15) 84 (65) 54 (127) 1 (1)

Species composition is designated by letters; a, pike; b, large sparsely rakered (LSR) whitefish; c, burbot; d, minnow (Phoxinus phoxinus); e,

grayling; f, Alpine bullhead (Cottus poecilopus); g, ruffe; h, roach (Rutilus rutilus); i, perch; j, ide (Leuciscus idus); k, densely rakered (DR)

whitefish; l, brown trout; m, vendace. Mean (�SD) density (n net series�1 h�1) and biomass (g net series�1 h�1) of key fish species recorded

during the study are presented.

*Water quality data courtesy of S. Taipale.

†Data from Lapland Centre for Economic Development, Transport and Environment.



analysis of diet, growth and carbon (d13C) and nitrogen

(d15N) stable isotope ratios.

Laboratory analysis

Piscivory by perch is common in the study area (Amund-

sen et al., 2003). However, the focus of this study was

ecological interactions among whitefish, ruffe and perch,

which may use similar invertebrate prey resources. As

piscivory is rare in whitefish and ruffe, perch whose

stomachs contained fish were considered piscivorous

and analysed independently of the rest of the sample.

Individual stomach fullness was visually estimated

using the points method (Hynes, 1950) on a scale of

0–10 (0 = empty, 10 = extended full stomach). Relative

volumetric proportions of different prey categories were

estimated. Stomach contents were divided into eight

categories: chironomid larvae, trichoptera larvae, small

benthic crustaceans, large benthic crustaceans (Asellus

aquaticus and Gammarus lacustris), Mollusca (Valvata sp.,

Lymnaea sp. and Pisidium sp.), pelagic zooplankton

(Bosmina sp., Daphnia sp., Calanoida, Cyclopoida), sur-

face insects (insect pupae & adults) and other rare prey

items (macrophytes, Hydracarina, Polyphemus pediculus,

Hirudinea, biofilm and decomposed material). The rela-

tive volume of each category was calculated for each fish

population. Body size of zooplankton and diameter of

molluscs (10 random individuals per fish, when avail-

able) were subsequently measured to identify variations

in prey size selectivity between native and invasive fish

species (Kahilainen et al., 2007).

A small piece of muscle tissue was excised from the dor-

sal flank of a subsample of each species for stable isotope

analysis. Sample sizes of whitefish, ruffe and perch varied

between 44 and 75 individuals per species. In addition, all

pike captured (n = 15–28 per lake) were analysed. All iso-

tope samples were freeze-dried, ground to a fine powder

and weighed (0.5–0.6 mg) in aluminium foil cups. d13Cand d15N values were recorded using FlashEA 1112 ele-

mental analyser coupled to Thermo Finnigan DELTAPLUS

Advantage mass spectrometer (for details see Fry & Sherr,

1984). Fish d13C values were arithmetically lipid norma-

lised to remove the influence of variable lipid concentra-

tions prior to data analysis (Kiljunen et al., 2006). d13C and

d15N values were obtained for each macroinvertebrate

family recorded at each depth along the transect. In

instances where too few individuals were obtained to

provide an effective sample size (0.5–0.6 mg), samples

from neighbouring depths were pooled. Mean littoral and

profundal values, based on the light compensation point

in each lake, were subsequently calculated from the

macroinvertebrate family values at the relevant depths.

Zooplankton samples from multiple vertical tows were

pooled to obtain sufficient sample weight (0.5–0.6 mg).

Data analysis

Growth rates of whitefish were calculated from length-

at-age data determined from burnt and cracked otoliths

(Bagenal & Tesch, 1978). As the data were not normally

distributed, mean length-at-age values between systems

were compared using pairwise Welch’s t-test, an ana-

logue of the Student’s t-test without the requirements

for similarities of variance. Welch’s t-tests were per-

formed in R (R Development Core Team, 2012). Fulton

condition factor (k) of each whitefish was determined

according to Bagenal & Tesch (1978):

k ¼ M

TL3

� �� 100

where M is the blotted fish mass (g) and TL is the total

fish length (cm). Variation in condition factors between

lakes and fish communities was assessed using Welch’s

t-test.

Variation in fish and invertebrate community struc-

ture and in the stomach content of fish was examined

using PERMANOVA (PRIMER 6.1.13; PRIMER-E, Plym-

outh, U.K.), a nonparametric permutation-based ana-

logue of analysis of variance between two or more

groups based on a distance measure (Anderson, 2001;

McArdle & Anderson, 2001). In each case, a Bray–

Curtis similarity matrix (Bray & Curtis, 1957) was created

from non-transformed abundance data. Two factor

PERMANOVAS were performed on the fish, macroinverte-

brate and zooplankton community structure similarity

matrices to test the effect of ‘lake’ (six levels, random)

and ‘fish community’ (three levels, fixed), with ‘lake’

nested within ‘fish community’, on variation within the

data set. A third factor, ‘species’ (three levels, fixed), was

included in the analysis of stomach content. In invaded

lakes, levels of dietary overlap were explored using pair-

wise PERMANOVA analysis. When significant variation

(P < 0.05) was observed between groups, percentage sim-

ilarity analysis (SIMPER) was used to determine which

prey items contributed most to the difference (Clarke,

1993). Comparisons of mean length of zooplankton and

small benthic crustaceans, and mean mass of macroinver-

tebrates between fish communities were performed using

Welch’s t-test.

The dietary niche of each species was calculated using a

standardised Levins’ index (Levins, 1968). As the value of

Levins’ index increases with sample size, niche width was



calculated based on the diet of a randomly selected sub-

sample of individuals (n = 30). Ontogenetic shift in perch

diet was examined using a Spearman’s rank correlation of

the proportion of fish in the stomach against total length

of perch. In addition, stomach content of the top con-

sumer, pike (n = 15–28 per lake), was examined to test the

degree to which they fed on native and invasive species.

Isotope values of consumers are largely defined by the

isotopic values of their prey, which may vary both spa-

tially and temporally (Syv€aranta, H€am€al€ainen & Jones,

2006). As such, between-lake analyses may be biased by

underlying variation and were not conducted in this

case. Levels of overlap between species stable isotope

ratios were determined using pairwise PERMANOVA analy-

sis of d13C-d15N centroids, based on a Euclidean distance

matrix created from the d13C and d15N values of white-

fish, ruffe and perch in each lake. Resource use of fish

was subsequently determined using stable isotope mix-

ing models (Boecklen et al., 2011). The relative impor-

tance of littoral, pelagic and profundal sources to each

species was calculated using the Bayesian mixing model

‘Stable Isotope Analysis in R’ (SIAR; Parnell et al., 2010).

Standard trophic fractionation values for muscle tissue

(D13C = 1.3 � 0.3, D15N = 2.9 � 0.3) were used in all

cases (McCutchan et al., 2003). Comparison of resource

use between species and systems was conducted by com-

paring the 95% credibility limits of each prey source, if

credibility limits did not overlap species were deemed to

be utilising the resource at significantly different levels.

The isotopic niche breadth of each species was calcu-

lated based on the standard ellipse of d13C-d15N space

(Jackson et al., 2011). To overcome the disparity in sam-

ple sizes, the area of a small-sample-size-corrected

ellipse (SEAc), calculated using ‘Stable Isotope Bayesian

Ellipses in R’ (SIBER; Jackson et al., 2011), was used to

determine isotopic niche size. Variation in niche size

between species was subsequently calculated using the

likelihood test in SIBER (Jackson et al., 2011). SIAR and

SIBER analyses were performed using the ‘SIAR pack-

age, version 4.1.3’, in R (R Development Core Team,

2012). Ontogenetic shifts in isotopic position of fish were

tested using a Spearman’s rank correlation of d13C and

d15N against total length of fish.

Results

Invertebrate community

Benthic macroinvertebrate abundance (n m�2) varied

between lakes (pseudo F3,45 = 5.8, P < 0.01), but variation

was not associated with fish community structure Tab

le2

Mean(�

SD)den

sity

ofben

thic

invertebrates(n

m�2)an

dpelag

iczo

oplankton(n

L�1)observed

innon-invad

ed(N

I),whitefi

shan

druffe(W

R)an

dwhitefi

shruffean

dperch

(WRP)lakes

Community

Lak

eHab

itat

Chiro

Tric

SBC

LBC

Moll

Oligo

Insecta

Hydra

Other

Cladocera

Copep

oda

NI

L.Kolta

Littoral

2464

(116

0)11

(21)

627(402

)11

(31)

222(215

)12

65(160

0)11

(21)

83(73)

83(73)

0.22

(0.31)

2.01

(1.18)

Profundal

––

––

––

––

––

–

L.Kuohkim

aLittoral

833(483

)20

(23)

30(89)

10(20)

168(213

)59

(86)

10(20)

10(30)

5(15)

0.46

(0.24)

4.21

(1.51)

Profundal

747(105

7)–

141(323

)67

(163

)81

(139

)22

(37)

–15

(36)

––

–

WR

L.Oiko

Littoral

1554

(491)

44(102)

705(621)

–30

6(165

)11

3(97)

25(32)

44(44)

5(15)

0.13

(0.08)

1.29

(0.77)

Profundal

969(103

0)1(18)

318(477

)–

59(61)

200(156

)–

81(114

)22

(24)

––

L.Ropi

Littoral

557(279

)49

(72)

508(242

)23

7(480

)10

9(74)

666(449

)10

(30)

123(125

)25

(32)

0.10

(0.01)

0.19

(0.03)

Profundal

170(190

)–

159(174

)–

41(61)

111(75)

––

––

–

WRP

L.Kivi

Littoral

2033

(1029)

59(104)

286(261)

5(15)

405(277)

409(464)

158(71)

44(54)

39(47)

0.19

(0.2)

0.13

(0.15)

Profundal

1066

(452

)–

311(348

)–

111(88)

178(225

)7(18)

44(40)

7(18)

––

L.Palo

Littoral

1374

(650

)55

(45)

3367

(352

6)13

5(177

)27

6(354

)43

5(191

)27

0(209

)14

1(133

)86

(50)

0.59

(0.48)

0.97

(0.23)

Profundal

––

––

––

––

––

–

Abbreviationsofben

thic

invertebratesreferto

chironomid

larvae

(Chiro),trichoptera

larvae

(Tric),sm

allben

thic

crustaceans(SBC;Ostracoda,

Eurycercussp

p.,Megacyclops

spp.),large

ben

thic

crustaceans(LBC;Asellusaquaticus,Gam

maruslacustris),molluscs(M

oll;Valvata

sp.,Lym

naeasp

.,Pisidium

sp.),Oligoch

aeta

(Oligo),Insecta(Ephem

eroptera,Sialisan

dPlecop-

tera)an

dHydracarina(H

ydra).In

lakes

containingaprofundal

zone,

ben

thic

invertebratesaresu

bdivided

into

littoralan

dprofundal.Pelag

iczo

oplanktonaresu

bdivided

into

clad

o-

cera

andcopep

oda.



(pseudo F2,45 = 0.7, P = 0.8; Table 2). Overall macroinver-

tebrate density was greater in WRP lakes than in WR

lakes (t = �3.9, d.f. = 34, P < 0.01). High variation

between both NI lakes (L. Kolta contained the highest

density recorded in the study and L. Kuohkima con-

tained the lowest density; Fig. 2a) obscured any differ-

ence between these and WR (t = 1.6, d.f. = 27.2,

P = 0.11) or WRP lakes (t = �0.77, d.f. = 34.7, P = 0.45).

Within-lake variation was evident as littoral macroinver-

tebrate density was higher than its profundal counter-

part in all lakes (pseudo F1,45 = 6.5, P < 0.01).

Zooplankton community structure (ind L�1) varied

between lakes (pseudo F3,17 = 6.2, P < 0.01; Table 2), but

this was unrelated to fish community structure (pseudo

F2,17 = 1.6, P = 0.24). Mean density of pelagic zooplank-

ton (Fig. 2a) was higher in NI lakes than in with WR

lakes (t = 3.1, d.f. = 6.8, P = 0.02) or WRP lakes (t = 3,

d.f. = 6.5, P = 0.02), although no variation was evident

between invaded lakes (t = �0.2, d.f. = 9.9, P = 0.85).

Mean zooplankton size decreased relative to fish diver-

sity (Fig. 2b). Zooplankton were smaller in WR lakes

than in NI lakes (t = 10.7, d.f. = 525.3, P < 0.01). Simi-

larly, zooplankton in WRP were smaller than in WR

lakes (t = 8.6, d.f. = 450.1, P < 0.01). Measurements were

not available for small benthic crustaceans in Lake Palo

but the populations in Lake Kivi contained smaller indi-

viduals than those in NI (t = 2.6, d.f. = 0.01, P < 0.01)

and WR lakes (t = 3.4, d.f. = 164.5, P < 0.01). No

variation in mean size was evident between small ben-

thic crustaceans in NI and WR lakes (t = 3.4, d.f. =

149.6, P = 0.28; Fig. 2b). Mean macroinvertebrate mass

did not vary between fish communities (P > 0.05 in all

cases; Fig. 2b).

Fish community

Two perch were recorded from Lake Ropi, indicating that

the species may be beginning to establish in this lake;

however, this was not deemed sufficient to reclassify the

lake. Significant variation in fish community structure

(CPUE) was evident between lake types (pseudo

F3,37 = 2.7, P < 0.04), principally due to variation between

NI and WRP lakes (Table 1; t = 2.3, d.f. = 2, P = 0.02).

Proportional composition of whitefish decreased from c.

90% in NI lakes (mean � SD: L. Kolta: 88 � 9%; L. Ku-

ohkima: 89 � 8%) to a lower proportion in WR lakes (L.

Oiko: 74 � 14%; L. Ropi: 16 � 20%) and WRP lakes (L.

Kivi: 42 � 15%; L. Palo: 10 � 7%). Whitefish density var-

ied between lakes but this variation was not associated

with fish community structure (Fig. 3a). Whitefish

2000

4000

6000

8000 BMI

0

0.025

0.05

0.075

0.01

Mea

n in

divi

dual

mas

s (g

)L. Kolta L. Kuohkima L. Oiko L. Ropi L. Kivi L. Palo L. Kolta L. Kuohkima L. Oiko L. Ropi L. Kivi L. Palo

2000

4000

6000

8000 SBC SBC

Leng

th (m

m)

2

4

6

8

Den

sity

(n l–

1 )D

ensi

ty (n

m–2

)D

ensi

ty (n

m–2

)10 ZPL ZPL

0

0.5

1

1.5

2

Leng

th (m

m)

BMI

LittoralProfundal

0

0.5

1

1.5

2

(a) (b)

Fig. 2 (a) Density and (b) mean size of zooplankton (ZPL; Bosmina sp., Daphnia sp., Calanoida, Cyclopoida), small benthic crustaceans (SBC;

Ostracoda, Eurycercus spp., Megacyclops spp.) and benthic macroinvertebrates (BMI) in non-invaded (L. Kolta, L. Kuohkima), whitefish and

ruffe (L. Oiko, L. Ropi), and whitefish, ruffe and perch (L. Kivi, L. Palo) lakes. Error bars indicate 95% confidence limits.



biomass (g net series�1 h�1) was indistinguishable

between NI and WRP lakes (t = 1.2, d.f. = 12.3, P = 0.27),

but reduced biomass was observed in WR lakes relative

to both NI (t = 2.8, d.f. = 10.7, P = 0.01) and WRP

(t = �2.6, d.f. = 26.9, P = 0.01) lakes (Table 1; Fig. 3b).

Mean total length of whitefish also varied between fish

communities; whitefish in NI lakes (mean � SD:

25.3 � 7.4 cm) were larger (t = 10.7, d.f. = 362.2,

P < 0.01) than those in WR (14.8 � 4.7 cm) lakes and WRP

(17.3 � 7.8 cm) lakes (t = 10.5, d.f. = 287.9, P < 0.01). Mean

size of whitefish in WRP lakes was larger than in WR

lakes (t = �6.7, d.f. = 675.5, P < 0.01).

A decrease in mean condition factor (k) of whitefish was

observed between NI and WR lakes (Fig. 3c; t = 3.2,

d.f. = 239.8, P < 0.01). Condition of whitefish was lower in

WRP lakes than inWR lakes (t = �8.8, d.f. = 187, P < 0.01).

However, significant variation was evident between the

two study lakes in the latter category (t = �23.5,

d.f. = 129.6, P < 0.01); whitefish in Lake Kivi exhibited the

lowest condition (mean � SD: 0.7 � 0.1), while the highest

condition factor was observed in Lake Palo (1.2 � 0.15).

The highest growth rates of whitefish were observed

in Lakes Palo and Kolta (Table S2; Fig. 3d). Growth of

whitefish was unrelated to fish community structure.

Significant variation was observed between pairwise

length-at-age values of whitefish in the replicate lakes in

NI (t = 3.5, d.f. = 5, P = 0.02), WR (t = �2.9, d.f. = 7,

P = 0.02) and WRP (t = �7.7, d.f. = 6, P < 0.01) systems.

L. Kolta L. Kuoh L. Oiko L. Ropi L. Kivi L. Palo0.5

0.75

1

1.5

1.25

Lake

Con

ditio

n fa

ctor

(k)

(b)

Age1 2 3 4 5 6 7 8

Tota

l len

gth

(mm

)

0

100

200

300

400

500

(c)

L. Kolta L. Kuoh L. Oiko L. Ropi L. Kivi L. Palo

10

20

30

0

Den

sity

(n n

et s

erie

s–1

h–1 )

(a)

L. Kolta L. Kuoh L. Oiko L. Ropi L. Kivi L. Palo

(d)

Bio

mas

s (1

000

g ne

t ser

ies–

1 h

–1)

0

1

2

3

4

Lake Lake

WhitefishRuffePerchOther

L. KoltaL. KuohL. OikoL. RopiL. KiviL. Palo

Fig. 3 Characteristics of fish populations in non-invaded (L. Kolta & L. Kuohkima), whitefish and ruffe (L. Oiko & L. Ropi) and whitefish,

ruffe and perch (L. Kivi & L. Palo) lakes. (a) Mean density (catch per unit effort) and (b) biomass of large sparsely rakered whitefish, ruffe,

perch and combined other species. (c) Boxplots of condition factor (k) of whitefish. Median value is denoted by a horizontal line, box out-

lines upper and lower quartiles, and outliers are represented as circles. (d) Mean total length-at-age of whitefish. L. Kuohkima is abbreviated

to L. Kuoh for illustrative purposes.



Stomach contents

Whitefish and percids utilised distinct prey resources

across all systems (pseudo F1,2 = 6.2, P < 0.01). In each

lake, the diet of ruffe was distinguished from that of

whitefish and perch by a higher proportion of chirono-

mid larvae and large crustaceans (Table 3; Fig. 4). Varia-

tion between whitefish and perch was largely due to an

increased abundance of small benthic crustaceans in

whitefish diet relative to perch.

The diet of whitefish did not differ between fish com-

munities (pseudo F2,486 = 0.99, P = 0.53), but variation in

diet between lakes within each community type was

observed (pseudo F3,486 = 15.9, P < 0.01). Similarly, the

diet of ruffe was unaffected by the presence of perch

(pseudo F1,420 = 2.1, P = 0.19), although lake-specific vari-

ations were evident (pseudo F2,420 = 24.8, P < 0.01).

Mean prey size of whitefish (1.95 mm) was larger than

that of ruffe (1.74 mm), at a close to significant level

(t = 2.04, d.f. = 13, P = 0.06). Prey size did not vary sig-

nificantly between whitefish and perch (t = 0.84, d.f. = 3,

P = 0.46) or between perch and ruffe (t = 0.17, d.f. = 4,

P = 0.87). No variation in niche width was evident

between whitefish and ruffe (t = �0.65, d.f. = 3,

P = 0.56). Where present, perch utilised a broader niche

than whitefish (t = �28, d.f. = 1, P = 0.02) and had a sim-

ilar niche width to ruffe (t = �1.91, d.f. = 1, P = 0.31).

An ontogenetic shift to piscivory was evident in the

diet of perch. The proportion of fish in the stomach was

correlated with total length in Lake Kivi (rs = 0.53,

n = 99, P < 0.01) and Lake Palo (rs = 0.65, n = 40,

P < 0.01). The minimum size of piscivorous perch (i.e.

perch with fish prey in their stomach) was 162 mm in

Lake Kivi and 150 mm in Lake Palo. In perch over

150 mm, fish prey comprised 70 � 44% of stomach con-

tent in Lake Kivi and 77 � 42% in Lake Palo. Whitefish

was the most common prey (43 � 48%) in the stomach

content of piscivorous perch, considerably outnumbering

ruffe (6 � 23%). Whitefish was the most common prey

source of pike in Lakes Oiko (61 � 49%; n pike = 27),

Ropi (54 � 55%; n = 22), Kivi (45 � 49%; n = 18) and

Palo (48 � 50%; n = 14). Ruffe were recorded in pike

stomachs in Lakes Oiko (6 � 17%) and Kivi (12 � 35%),

while perch were not found in any pike stomachs. No

fish prey was found from ruffe or whitefish stomachs.

Stable isotope analysis

Pairwise PERMANOVA revealed trophic segregation

between species in most cases (Table 4; Fig. 5). In both

WR lakes, ruffe displayed a higher d15N value than

Tab

le3

Mean(�

SD)relativeproportion(%

)ofpreygroupsin

thestomachcontents

ofwhitefi

sh(W

),ruffe(R)an

dperch

(P)

Community

Lak

eSpecies

nChiro

Tric

SBC

LBC

Moll

Insecta

Other

ZPL

T.insect

Fullness

Lev

ins

PERMANOVA

NI

L.Kolta

Whitefi

sh80

6(10)

7(21)

16(26)

<1(1)

4(15)

4(15)

1(15)

51(44)

10(23)

4.3

0.45

L.Kuohkim

aW

hitefi

sh11

99(19)

5(19)

42(40)

–16

(25)

2(12)

–11

(28)

15(29)

3.7

0.48

WR

L.Oiko

Whitefi

sh15

03(9)

–52

(39)

<1(<1)

25(34)

<1(<1)

<1(<1)

16(32)

3(13)

3.7

0.27

W*R

P<0.01

Ruffe

171

11(15)

17(23)

57(31)

6(17)

3(8)

2(7)

<1(<1)

4(16)

–4.5

0.24

L.Ropi

Whitefi

sh77

4(14)

6(21)

35(39)

5(15)

30(35)

<1(<1)

2(1)

11(30)

7(23)

2.4

0.43

W*R

P<0.01

Ruffe

7415

(27)

2(10)

50(37)

23(33)

6(13)

–2(12)

2(7)

–3.9

0.31

WRP

L.Kivi

Whitefi

sh57

3(8)

4(16)

50(42)

–17

(29)

2(8)

4(16)

19(37)

1(6)

2.8

0.26

W*R

P<0.01

Ruffe

9121

(24)

8(18)

15(21)

32(38)

5(12)

1(11)

1(1)

17(19)

–4.3

0.39

W*P

P<0.01

Perch

150

–40

(45)

9(27)

4(17)

11(28)

9(25)

16(37)

11(29)

–2.7

0.55

P*R

P<0.01

L.Palo

Whitefi

sh75

<1(2)

<1(2)

76(22)

3(11)

19(18)

<1(1)

–1(6)

–6.3

0.08

W*R

P<0.01

Ruffe

155

18(18)

4(1)

36(35)

37(29)

<1(1)

3(7)

–2(11)

–5.7

0.30

W*P

P<0.01

Perch

471(6)

10(27)

41(37)

––

6(23)

20(32)

21(33)

<1(2)

3.7

0.35

P*R

P<0.01

Abbreviationsreferto

chironomid

larvae

(Chiro),trichoptera

larvae

(Tric),sm

allben

thic

crustaceans(SBC),largeben

thic

crustaceans(LBC)an

dmolluscs(M

oll),zo

oplankton(ZPL)

andterrestrialinsects(T.insect).Other

includes

macrophytes,

Hydracarina,

Polyphemuspediculus,Hirudinea,biofilm

anddecomposedmaterial.Estim

ationofstomachfullness(1–10),

stan

dardised

Lev

insindex

ofnichewidth

and

PERMANOVAcomparisonsofdietary

overlapareincluded

,instan

cesofsignificantvariationin

dietarehighlightedin

bold.



whitefish (Table 4). This segregation in d15N was also

evident in Lake Kivi, whereas in Lake Palo, the differ-

ence was marginally significant (Table 4). Ruffe also dis-

played elevated d15N relative to perch in Lake Kivi, but

not in Lake Palo (Fig. 5). Variation observed in Lake

Palo was primarily due to differences in d13C (Table 4).

The isotopic values of perch and whitefish were statisti-

cally indistinguishable in Lake Kivi, while in Lake Palo

perch were depleted in d13C relative to whitefish

(Table 4). SIBER ellipses revealed increased levels of

overlap between the isotopic niches of native and inva-

sive species in lakes with increased species diversity,

especially in Lake Kivi (Fig. 5). Isotopic niche size varied

considerably between species, although no species

employed a characteristically smaller or larger niche

than any other across all lakes (Table 4). Stable isotope

values revealed pike to be the apex predator in all sys-

tems; mean d13C values of pike were intermediate

between perch, ruffe and whitefish, while d15N was ele-

vated relative to all other species except in Lake Ropi,

where ruffe had the highest d15N values.

The isotope mixing model identified overlapping

resource use between species in most invaded lakes

(Table 4, Fig. 6). Resource segregation was most evident

in WR lakes. In Lake Oiko, levels of littoral resource use

differed between whitefish and ruffe, however profun-

dal and pelagic resource use of either species were

within the 95% credibility limits of the other (Table 4,

Fig. 6). In Lake Ropi, whitefish predominantly utilised

littoral resources, while ruffe were more closely aligned

with the profundal (Table 4, Fig. 6). Resource segrega-

tion was less evident in WRP lakes as resource use of all

species was within the 95% credibility limits (Fig. 6).

Ontogenetic variation in isotopic position was not evi-

dent in the majority of cases (Table 4). In whitefish, d13Cvalues increased over ontogeny in Lake Kolta, while an

increase in d15N was evident in Lake Palo, both probably

associated with the diet shift from zooplankton to ben-

thic macroinvertebrates. d15N values were strongly cor-

related with total length in both perch populations,

indicating a diet shift from invertebrates to fish.

Discussion

The invasion of percids did not alter the benthic macroin-

vertebrate community structure or density directly, but

indirectly lowered zooplankton density and size. This

apparently was not due to a direct niche shift of whitefish

into the pelagic habitat. There was some evidence of low-

ered condition, mean length and population size of white-

fish in invaded lakes, suggesting that whitefish may face

increased levels of resource competition following inva-

sion. In general however, the invading percids showed

niche segregation with native whitefish. Thus, in an early

Chiro LBC SBC ZPL Other

L. Palo

0

L. Kivi

50

100

Abu

ndan

ce (%

)

L. RopiL. Oiko

L. KuohkimaL. Kolta

Chiro LBC SBC ZPL Other

0

50

100

0

50

100

0

50

100

0

50

100

0

50

100WhitefishRuffePerch

Non-invaded (NI)

Whitefish & ruffe (WR)

Whitefish, ruffe & perch (WRP)

Fig. 4 Proportional abundance of key prey groups in the stomach contents of whitefish, ruffe and perch in non-invaded, whitefish and

ruffe, and whitefish, ruffe and perch lakes. Prey groups are summarised as chironomid larvae (Chiro), large benthic crustaceans (LBC;

Asellus aquaticus, Gammarus lacustris), small benthic crustaceans (SBC; Ostracoda, Eurycercus spp. & Megacyclops spp.), zooplankton (ZPL;

Bosmina sp., Daphnia sp., Calanoida, Cyclopoida) and other prey (other; Trichoptera, Valvata sp., Lymnaea sp., Pisidium sp., Hydracarina,

Polyphemus pediculus, Hirudinea, insect larvae, pupae and adults). Error bars represent 95% confidence limits.



Table

4Mean(�

SD)stab

leisotopevalues

ofwhitefi

sh(W

),ruffe(R),perch

(P)an

dpike.

Community

Lak

eSpecies

nd1

3C‰

d15N‰

d13C

r sd1

5N

r sPERMANOVA

Littoral(%

)Pelag

ic(%

)Profundal

(%)

SEAc

Nichesize

NI

L.Kolta

Whitefi

sh50

�21.6(1.4)

5.4(0.3)

0.86

�0.12

93(87–99

)7(1–13)

–1.3

Pike

16�2

2.3(1.1)

6.9(0.9)

L.Kuohkim

aW

hitefi

sh50

�26.1(2.5)

6.9(0.6)

0.12

�0.27

29(22–36

)71

(64–78

)–

4.8

Pike

15�2

4.4(1.0)

8.0(0.7)

WR

L.Oiko

Whitefi

sh50

�28.5(2.2)

8.0(0.4)

0.3

�0.14

W*R

P<0.01

22(11–29

)9(0–26)

69(57–78

)2.1

W*R

P=0.03

Ruffe

44�2

7.9(1.5)

9.3(0.4)

0.41

0.3

37(28–44

)2(0–17)

61(43–71

)1.7

Pike

2827

.4(0.8)

9.7(0.8)

L.Ropi

Whitefi

sh50

�22.8(1.7)

6.8(0.5)

0.21

�0.16

W*R

P<0.01

70(63–76

)1(0–4)

29(23–36

)2.4

W*R

P<0.01

Ruffe

44�2

4.8(2.5)

8.3(0.7)

0.37

�0.46

35(30–40

)2(0–7)

63(57–68

)4.7

Pike

22�2

4.0(1.6)

7.9(0.8)

WRP

L.Kivi

Whitefi

sh44

�25.4(1.9)

7.7(0.5)

�0.17

0.47

W*R

P<0.01

77(67–86

)2(0–9)

21(10–30

)2.8

W*R

P=0.72

Ruffe

44�2

4.4(1.8)

8.9(0.6)

�0.08

�0.27

W*P

P=0.22

89(81–96

)2(0–8)

9(1–16)

3.4

W*P

P=0.01

Perch

50�2

5.0(0.9)

7.5(0.5)

0.44

0.93

R*P

P<0.01

86(72–95

)3(0–14)

11(1–23)

1.4

R*P

P=0.01

Pike

18�2

5.0(0.7)

9.7(0.7)

L.Palo

Whitefi

sh75

�24.4(0.8)

5.7(0.6)

�0.1

0.86

W*R

P=0.06

54(46–62

)46

(38–54

)–

1.6

W*R

P=0.01

Ruffe

60�2

4.2(0.3)

5.5(0.4)

0.1

0.39

W*P

P<0.01

50(40–59

)50

(41–59

)–

0.4

W*P

P=0.01

Perch

46�2

5.8(1.4)

5.6(0.7)

�0.1

0.7

R*P

P<0.01

45(34 –54

)55

(46–66

)–

3.2

R*P

P<0.01

Pike

15�2

5.5(1.4)

6.9(1.2)

Spearm

an’s

rankcorrelations(rs)ofisotopic

positionan

dfish

totallength,PERMANOVA

comparisonsofcentroid

isotopic

positionareprovided

forwhitefi

sh,perch

andruffe.Mean

(95%

Bay

esiancred

ibilityintervalsin

paren

theses)relativeproportionoflittoral,pelag

ican

dprofundal

preyresourceas

determined

bytheStable

IsotopeAnalysisin

Rmixingmodel

aresh

own,note

theab

sence

ofaprofundal

zonein

Lak

esKolta,

Kuohkim

aan

dPalo.A

measu

reofisotopic

nichewidth

(SEAc)

andapairw

isecomparisonofnichewidth

arealso

displayed

.Statistically

significantvalues

(P<0.05)arehighlightedin

bold.



phase of the percid invasion, there seems to be surpris-

ingly low impacts on the native ecosystem.

Resource competition between species depends on

prey being a limiting factor and is notoriously difficult

to prove. However, effects of competing consumers may

be evident in the prey community as a shift in commu-

nity structure towards smaller species and a size struc-

turing of the prey population towards smaller

individuals (Bøhn et al., 2008). Our results indicate that

neither effect was evident within the benthic macroin-

vertebrate communities in the studied lakes. Macroin-

vertebrate density was higher in WRP lakes than in WR

δ15N

0

2

4

6

8

10

12 L. Oiko

0

2

4

6

8

10

12

–35 –30 –25 –20 –15 –35 –30 –25 –20 –15

δ13C

0

2

4

6

8

10

12 L. Kolta L. Kuohkima

L. Ropi

L. Kivi L. Palo

WhitefishRuffePerch

Non-invaded (NI)


Whitefish, ruffe & perch (WRP)

Fig. 5 Isotope bi-plot including standard ellipses denoting the isotopic niche width (SEAc) of large sparsely rakered whitefish, ruffe and

perch. Mean (�SD) values of littoral (triangle), pelagic (square) and profundal (circle) zones are also provided. Note the lack of profundal in

L. Kolta, Kuohkima and L. Palo.



lakes, while densities in the replicate NI lakes included

the highest (Lake Kolta) and the lowest (Lake Kuohk-

ima) values observed in the study. The density of small

benthic crustaceans was similarly unrelated to fish com-

munity structure, with the highest recorded density

found in Lake Palo. Invertebrate community structure

reflects a complex interaction between lake-specific pro-

ductivity and predator communities (Diehl, 1992; Town-

send, 2003), and the reported scenario, where resident

and invasive fish populations are maintained by the

same resource, suggests that benthic prey were not a

limiting resource (Hayden et al., 2011). In contrast, it is

apparent that the pelagic zooplankton community is

under top-down control, suggesting increased predation

intensity in the invaded systems. The highest zooplank-

ton densities were recorded in NI lakes, and there was

clear size structuring between zooplankton communities,

with a smaller mean size recorded in invaded systems.

These trends concur with previously evidence of preda-

tion by efficient zooplanktivorous coregonid fishes (Bøhn

& Amundsen, 1998).

We predicted that perch and ruffe would dominate

benthic food resources in each system, leading to a shift

towards pelagic feeding in whitefish. While both percid

species were strongly associated with benthic feeding in

each lake, their presence did not result in increased pela-

gic foraging by whitefish. Results of the stable isotope

mixing model indicate that in invaded systems, all three

fishes fed in the same food-web compartment. Dietary

segregation between the species was evident in the

stomach contents, although this was typically related to

a division of benthic prey items and rarely involved a

shift towards pelagic feeding by whitefish. In WR lakes,

the species were distinguished by enriched d15N values

of ruffe. These results are consistent with utilisation of a

greater proportion of profundal prey, which typically

have enriched d15N values (Harrod & Grey, 2006). Such

a division of resources allows both species to feed pri-

marily on the benthos, as evident in the stomach content

data, while maintaining an element of resource segrega-

tion. Whitefish are principally a visual predator, whereas

ruffe have adaptations enabling them to feed efficiently

in dark conditions (Disler & Smirnov, 1977; Schleuter &

Eckmann, 2006), facilitating more efficient use of the

profundal zone. There is further evidence of resource

segregation in lakes containing all three species. In Lake

Kivi, ruffe were distinguished from both whitefish and

perch by enriched d15N values, again indicative of

increased use of profundal resources, although this was

not evident in the results from the SIAR mixing model.

In Lake Palo, the opportunity for resource segregation

was restricted due to the absence of a distinct profundal

zone. However, perch exhibited depleted d13C values

relative to both whitefish and ruffe, while dietary segre-

gation in stomach contents was also evident between the

species.

L. Kivi L. Palo

L. KuohkimaL. Kolta

Pelagic Littoral Profundal Pelagic Littoral Profundal

0

0.6

0.2

0.4

0.8

1

L. RopiL. Oiko

(a)

(b)

(c)

noitubirtnoC

noitubirtnoC

noitubirtnoC

0

0.6

0.2

0.4

0.8

1

0

0.6

0.2

0.4

0.8

1

Non-invaded (NI)


Whitefish, ruffe and perch (WRP)

WhitefishRuffePerch

Fig. 6 Relative contributions of pelagic, littoral and profundal resources to the isotopic values of whitefish, ruffe and perch (WRP) in (a)

non-invaded, (b) whitefish and ruffe, and (c) whitefish, ruffe and perch lakes. Note the lack of profundal in L. Kolta and L. Palo. Gradations

denote 50, 75 and 95% credibility limits.



Lake-specific factors influenced resource availability in

the invaded systems, potentially dictating the opportuni-

ties for resource segregation. Two of the invaded lakes

contained a pelagic specialist, the DR morph of white-

fish in Lake Ropi and vendace in Lake Palo. Both DR

whitefish and vendace are more efficient zooplankti-

vores than LSR whitefish and may exclude them from

pelagic feeding (Bøhn & Amundsen, 2001; Harrod et al.,

2010). As such, pelagic resources were not available to

LSR whitefish in these lakes and could not be used to

avoid resource competition with percids. The bathymet-

ric differences between lakes also influenced niche avail-

ability for the entire fish fauna. The lack of pelagic zone

in Lakes Kolta, Kuohkima and Palo forced all the fish

species to forage in the littoral, while the low amount of

pelagic habitat in Lakes Oiko and Kivi limited LSR

whitefish’s ability to shift to planktivory.

We predicted that effects of resource competition

would be evident in the life-history characteristics of

native whitefish in invaded lakes. However, lake-specific

factors such as bathymetry and productivity appear to

govern the effect of increased competitor diversity on

the population size, growth and condition of native

whitefish. Whitefish density was unrelated to fish com-

munity structure. While the proportion of whitefish stea-

dily declined in parallel with invader densities, invaded

lakes exhibited both the highest and the lowest whitefish

densities recorded in the study. Biomass of whitefish

also displayed evidence of site-specific variation. While

reduced biomass was evident in WR lakes, the biomass

of whitefish in WRP lakes was similar to that found in

NI systems. Whitefish growth was fastest in Lakes Kolta

and Palo, which are both shallow and contained high

benthic macroinvertebrate densities. Condition factor of

whitefish showed clear variation according to fish com-

munity structure. Increased competitor diversity corre-

sponded with a decrease in the relative condition of

whitefish, although the highest condition factor was

observed in mesotrophic Lake Palo.

The effect of this lake-specific variation is difficult to

thoroughly determine due to differences between repli-

cate lakes. Lake Palo is an outlier in some respects as it

is considerably more productive than the other lakes.

Increased nutrient load facilitates a greater density of

invertebrate prey items, probably accounting for the ele-

vated growth and condition of whitefish in the presence

of numerous competitors. In addition, Lake Palo was

sampled in 2009, two years earlier than the other lakes.

While this scenario is not ideal, previous studies of

whitefish in this region revealed a high comparability of

dietary results from different years (Kahilainen et al.,

2004; Harrod et al., 2010; Hayden, Harrod & Kahilainen,

2013). In addition, our samples were obtained from each

lake during late summer; consequently, we cannot

account for potential seasonal variation in diet and asso-

ciated dietary overlap. Lakes in this region are ice cov-

ered for six months per year, limiting primary

production and the density of zooplankton (Forsstr€om

et al., 2005). Under these conditions, the diet of whitefish

switches from a broad generalist during the open-water

season to one dominated by benthic prey in winter

(Hayden et al., 2013). This may increase the likelihood of

dietary overlap with benthivorous percids during the

winter period. Further research is currently underway to

address this issue; however, based on the data presented

here, it is evident that dietary overlap between native

and invasive species is not the case in invaded lakes

during the summer growing season.

Length-at-age data indicates that percid species have

been present in these lakes throughout the lifespan of the

current population of whitefish. However, the current sit-

uation is likely to present the early phase of invasion. The

invasion time of percids to these lakes is unknown, but

reports from fishermen in Lake Kivi suggest that percid

species are recent arrivals to this previously whitefish-

dominated system. As such, both species can be consid-

ered as still establishing in the region, and competition

for resources will probably increase as they become more

numerous (Colautti & Macisaac, 2004). The high overlap

in resource use between perch and whitefish, in conjunc-

tion with the highest density of perch observed in Lake

Kivi, indicates that increased percid density may result in

increased competition between native and invasive

fishes. Additionally, higher ruffe densities may have an

impact on native whitefish via egg predation (Winfield

et al., 1998), while increased predation on juvenile white-

fish by perch may have an impact on whitefish popula-

tion densities. Stable isotope and stomach content data of

pike indicate a greater reliance on whitefish than percids

as a prey source. Previous studies of selective predation

by pike in this region indicated strong preference for

whitefish (Amundsen et al., 2003; Kahilainen & Lehtonen,

2003), suggesting that densities of invasive percids in the

study lakes are not enough to change pike prey selection

from native whitefish, although this may change as the

invasion progresses. Ruffe is known to reach very high

population densities after establishment (Adams &

Maitland, 1998), and further investigations in the lower

reaches of the Tornio–Muoniojoki catchment, which con-

tains higher densities of both percid species (K. K. Kahi-

lainen unpublished data), would give better

understanding of the likely future scenario.



Data presented here suggest that specialist adaptations

allow moderate densities of invading species to be

subsumed into novel ecosystems before direct resource

competition with native taxa occurs. Determining the

point at which ecosystems become saturated, resulting

in resource competition deleterious to the native popula-

tions, is of key importance to understanding the ecologi-

cal impact of invasions. Future monitoring of these

populations may reveal how potentially changing inva-

der densities affect the interactions between native and

invasive taxa and any associated impacts upon the

native species (Simon & Townsend, 2003). Furthermore,

sampling of lower-latitude lakes in this catchment may

help explain how different densities of invasive species

influence the interactions with native species. Our find-

ings are particularly pertinent to the role of climate

change in determining future species range boundaries.

The carrying capacity of the lake ecosystem appears to

play a key role in regulating the impact of range expan-

sion on resident taxa. Moderate warming will probably

increase productivity levels in subarctic latitudes (Elliott,

Jones & Thackeray, 2006), and in addition, a longer

growing season and increased terrestrial vegetation will

indirectly increase the nutrient load in subarctic lakes

(Karlsson, Jonsson & Jansson, 2005). As such, a trade-off

may ensue whereby increased consumer density is med-

iated by increased resource availability. In effect, lakes

in this region represent a large biological experiment,

testing the interactions between resident and native spe-

cies in a habitat which is increasingly novel to both. This

provides a unique opportunity to examine the role

played by trophic ecology and resource competition as

the ecosystem reaches a new equilibrium.

In the systems, we assessed site-specific variations in

resource availability determine the outcomes of inva-

sions, defining the point where overlap in resource use

becomes resource competition. An assumption that

invading populations will de facto limit the resources

available to native species appears naive and should be

treated with caution. Rather the species interactions will

more likely be governed by variations in lake morphol-

ogy, productivity and community structure, leading to

an increasingly complex scenario of potential outcomes.

Acknowledgments

This manuscript was significantly enhanced by insight-

ful comments from two anonymous reviewers and the

journal editor. The study was financed by European

Regional Developmental Fund (A30205), Academy of

Finland (140903) and the Norwegian research council

(186320/V40). Authors thank C. Lien, K. Mankinen, P.

Nieminen, O. Saari and M. Sujala for the help in field

and laboratory work. Kilpisj€arvi Biological Station kindly

provided good facilities during the field work. KKK was

personally financed by Emil Aaltonen Foundation.

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Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Table S1. Mean (�SD) total length-at-age values (mm)

of whitefish, ruffe and perch.

Table S2. Mean (�SD) d13C and d15N isotope values (&)

of baseline invertebrates, including zooplankton (ZPL)

and benthic macroinvertebrates (BMI).

(Manuscript accepted 29 January 2013)



Interactions between invading benthivorous fish and native whitefish in subarctic lakes

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