Niche Characteristics Explain the Reciprocal Invasion Success of Stream Salmonids in Different Continents

Niche characteristics explain the reciprocal invasion success of stream salmonids in different continents

Kai Korsu*†, Ari Huusko‡, and Timo Muotka*§

*Department of Biology, University of Oulu, P.O. Box 3000, 90014, Oulu, Finland; ‡Finnish Game and Fisheries Research Institute, Kainuu Fisheries Research, Manamasalontie 90, 88300, Paltamo, Finland; and §Research Program for Biodiversity, Finnish Environment Institute, P.O. Box 413, 90014, Oulu, Finland

Edited by Ray Hilborn, University of Washington, Seattle, WA, and accepted by the Editorial Board April 12, 2007 (received for review December 5, 2006) An ability to understand and predict invasions is elemental for effects on lotic food webs (11), and it has been listed as one of controlling the detrimental effects of introduced organisms on the 100 worst alien species in the world by the Invasive Species native biota. In eastern North America, European brown trout Specialist Group. In contrast, there is no rigorous documenta- generally dominates over, and eventually replaces, the native tion of the impact of brook trout on native salmonids in brook trout. We show here that in northern Europe the pattern of European streams, although the species has been introduced to replacement between these two species is reversed: when trans- a number of streams throughout the continent (13, 14). Based on ferred to North European streams, brook trout spread extensively experience from North America, one might predict that brook and partially replaced the native brown trout. The effect of brook trout should be unable to establish populations if the competi- trout on brown trout was habitat-specific: brook trout excluded tively dominant native species, brown trout, is present. There- the native species only in small tributary streams where the fore, fisheries managers have assumed that brook trout does not reproduction of brown trout was severely reduced, whereas in pose a serious threat to brown trout or other native fish in larger streams brown trout was largely unaffected. Thus, the European streams (13). Here we show that biotic interactions pattern of coexistence among the two salmonids in our study area among stream salmonids can be strongly context-dependent and is approaching that typically observed in North American streams. that a species inferior in its native range can become an effective In both areas, brook trout ultimately settles in small headwater invader when transferred to areas where the presumably superior streams, but the process of replacement differs profoundly: in competitor is the native species, provided that the characteristics ECOLOGY North Europe, brook trout replaces brown trout in headwater of the new environment are favorable for the invader. streams, whereas in North America these same streams are the We collected our data from the headwaters and the main ultimate refuge area for brook trout under the invasion pressure by channel of the Upper Kemijoki River system, northeastern brown trout. Our results underline the importance of knowing Finland [see supporting information (SI) Fig. 4]. This stream species’ niche characteristics to explain and predict biological system supports abundant populations of brown trout. Brook invasions. trout was introduced in the system in the 1970s and 1980s in multiple, nondocumented events, but introductions ceased by alien species ͉ biological invasions ͉ trout the mid 1980s. We sampled fish in first-to-fourth order streams twice, in 1994 and 2004. We assessed fish densities using nvasions by alien organisms pose a global threat to biodiver- electroshocking and measured several habitat variables at each Isity, ecosystem functioning, and even human health (1). Spe- sampling site to examine whether brook trout had spread during cies transportation beyond their natural ranges has resulted in the intervening years and whether the invasion success was multiple, and often unpredictable, changes to recipient ecosys- habitat-mediated. tems. Thus, an improved ability to predict invasions is one of the key challenges to invasion biology and, indeed, to ecology, in the Results near future (2, 3). Progress has already been made by, for By 1994, brook trout had established mainly in small, slightly acid example, identifying biological traits characteristic of successful tributary streams in the middle-reaches of the drainage system, invaders and of communities vulnerable to invasion (4). Re- whereas by 2004 it had invaded further toward the headwaters cently, niche modeling has been applied to predict the risk of (Fig. 1; see also SI Fig. 4). This upstream expansion was very invasion by alien organisms in relation to biological and envi- rapid, because the limit of brook trout distribution had shifted ronmental resistance of the host ecosystem (2). Ϸ20 km in 10 years, markedly reducing the allopatric refuge area Most studies on species invasions have been reactive by nature; of brown trout. The tributary stream populations probably acted i.e., hypotheses are proposed to explain invasions that have as high-density (up to 60 individuals per 100 m2) (Fig. 2A) already taken place. For example, the enemy release hypothesis sources for the recent expansion, which was targeted toward suggests that alien species may be universally superior in their habitats formerly occupied by brown trout only (Fig. 1). By 2004, new environments because they have left old enemies behind and brook trout had colonized 20 new sites in headwater sections of the new ones might not detect the invader as a potential threat the study system (Table 1 and SI Fig. 4), leaving only six of 30 (or resource) (1). Hence, alien species may have access to surplus small (Ͻ7 m wide) stream sites uninvaded by 2004. Of these six resources, resulting in superior ecological performance. How- sites, four were in remote headwaters outside the current ever, invasions can be highly context-dependent, making the distribution of brook trout. outcome of a single invasion event unpredictable, at least without firm knowledge of the ecology of the species and the environment considered (5). Author contributions: K.K., A.H., and T.M. designed research; K.K. performed research; K.K. Brown trout (Salmo trutta L.) is a European salmonid fish that analyzed data; and K.K., A.H., and T.M. wrote the paper. has been introduced to all major continents, often to the The authors declare no conflict of interest. detriment of the native fish fauna (6, 7). In eastern North This article is a PNAS Direct Submission. R.H. is a guest editor invited by the Editorial Board. America, brown trout generally dominates over, and eventually †To whom correspondence should be addressed. E-mail: kai.korsu@oulu.fi. replaces, the native brook trout (Salvelinus fontinalis Mitchill) This article contains supporting information online at www.pnas.org/cgi/content/full/ (7–10). Brown trout is also a dominant competitor in New 0610719104/DC1. Zealand and Japanese streams (11, 12), having far-reaching © 2007 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0610719104 PNAS ͉ June 5, 2007 ͉ vol. 104 ͉ no. 23 ͉ 9725–9729 Downloaded by guest on September 27, 2021 Fig. 1. Distribution of the study sites along the ﬁrst two principal components of the stream habitat data. Variation explained (%) and the highest loadings of the original variables are given for each axis. F, brook trout allopatric; ■, sympatric; ᮀ, brook trout invasion; E, brown trout allopatric. Site categories differed in PC1 scores (ANOVA, F3,58 ϭ 17.26, P Ͻ 0.001), with brook trout allopatric and sympatric sites having lower scores than other categories (Tukey’s test, P Ͻ 0.001). No differences were detected for PC2 (F3,58 ϭ 1.05, P ϭ 0.38).

The relative density of brook trout compared with brown trout had increased in both sympatric and newly invaded sites while total trout density (brook trout plus brown trout) remained constant (Fig. 2). Natural reproduction of brown trout, as Fig. 2. Total trout densities (means Ϯ 1 SE) (A) and brown trout/brook trout indicated by the presence of age-0 fish, was severely reduced in density ratios (100 ϭ brown trout only, 0 ϭ brook trout only; means Ϯ 1 SE) (B) the presence of brook trout, but only in small streams (Fig. 3). for the two study years. Total trout densities remained constant across years (repeated-measures ANOVA: F ϭ 0.22, P ϭ 0.64), whereas sites in different Of the other native fish species, only bullhead (Cottus gobio L.) 1,58 categories supported different ﬁsh densities (F3,58 ϭ 9.25, P Ͻ 0.001), with provided sufficient data for a meaningful analysis. Bullhead allopatric brook trout sites having the highest and allopatric brown trout sites densities remained constant across study years (repeated- having the lowest densities (Tukey’s test, P Ͻ 0.01). The interaction term ϫ ϭ ϭ measures ANOVA: main effect of time, F1,39 ϭ 1.80, P ϭ 0.188), (year site category) was not signiﬁcant (F3,58 0.58, P 0.63). Brook trout whereas sites lacking brook trout in both years supported higher had increased its abundance compared with brown trout in sympatric sites ϭϪ ϭ densities of bullhead than those invaded by brook trout by 2004 (paired t test: t10 2.99, P 0.01). (main effect of site category, F1,39 ϭ 6.98, P ϭ 0.012). Impor- ϫ tantly, however, the interaction term (time site category) was Successful invaders often have novel ecological traits that ϭ ϭ insignificant (F1,39 1.30, P 0.261), indicating that brook trout make them superior competitors in the new environment (15). invasion did not directly modify bullhead densities. For example, brown trout has replaced native galaxids in New Interestingly, most (75%) of the newly invaded sites were in Zealand streams because invertebrate prey are much more relatively large streams (see Table 1), but it is doubtful whether vulnerable to this evolutionarily novel predator than to native these sites will meet the habitat requirements of brook trout in fish (11). However, the trout species studied by us are both the long term. In fact, all newly invaded sites lacking age-0 brook visually hunting, drift-feeding fish, and replacing brown trout trout were main-channel sites (mean stream width 16.7 m). with brook trout is unlikely to modify profoundly the predation Moreover, some main-channel populations had already disap- regime of stream invertebrates. Obviously, however, we cannot peared (n ϭ 7, mean stream width 18.8 m) between the study exclude the possibility that subtle differences in microhabitat years. Thus, occupation of the main-channel sites may represent selection and foraging tactics (16) might render the two species a transient phase in the ongoing invasion process that is directed sufficiently different, conferring a competitive edge for brook toward the upmost headwaters. trout in North European streams (and, conversely, for brown trout in North American streams). Discussion The fish fauna of North European streams is highly impov- Our data demonstrate that a subordinate native species can erished, as demonstrated by our study sites that supported on become a harmful invader when transferred to other systems average only three fish species (range 1–7). To this end, our data outside its native range. These data also show that the outcome might be interpreted as supporting the conventional notion that of biotic interactions can be highly context-dependent, and, when systems with low species richness are particularly susceptible to trying to understand the mechanisms of a successful invasion, or invasions. However, freshwater fish communities do not seem to to identify potential invaders a priori, one should have ample obey this rule, because there are numerous examples of intro- information about the invaded habitat, recipient biota, and niche duced fish becoming established in diverse assemblages (5). characteristics of the introduced species. More likely, it appears that brook trout, being an acid-tolerant

9726 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0610719104 Korsu et al. Downloaded by guest on September 27, 2021 Table 1. Site categorization based on the presence or absence of the two trout species in both study years Natural reproduction of Stream width, Site category n Description brook trout, % of sites m (range) pH (range)

Allopatric brook trout 5 Brook trout present, brown trout 100 3.3 (1.7–5.0) 6.3 (6.1–6.6) absent in both years* Sympatric 11 Both species present in both years 91 7 (2.6–16.1) 6.2 (4.9–7.2) Invasion 20 Brook trout present in 2004 but 70 11.8 (3.5–16.8) 6.8 (6.6–7.2) not in 1994, brown trout present in both years Allopatric brown trout 26 Brown trout present, brook trout 0 14.8 (3.7–40) 6.9 (6.3–7.2) absent in both years

Natural reproduction of brook trout is indicated as the percentage of sites where age-0 individuals were found. Means and ranges of key habitat variables for each site category are also given. *Brown trout occurred in very low numbers (one to three individuals per 100 m2) in some of these sites in either one of the study years.

headwater specialist (17–19), has colonized niche space only is less adapted to these extreme conditions. Indeed, this is exactly marginally used by any salmonid fish in North European streams. what has already happened in our sympatric and recently invaded Accordingly, we found brook trout mainly in small tributary tributary streams, where the natural reproduction of brown trout is streams characterized by harsh and variable environmental reduced to negligible levels. Thus, at the river-wide scale, the spatial conditions (20), whereas brown trout was prevalent in larger, pattern of coexistence among the two salmonid species is approach- more benign downstream sites (see also ref. 19). ing that typically observed in North American streams (17, 21). In In eastern North America, where brown trout has spread exten- both continents, brook trout ultimately settle in small headwater sively, headwater streams often serve as a refuge for brook trout streams, but the process of replacement differs profoundly: here (17, 21). In our study area, these upmost headwaters are now brook trout replace brown trout in headwater streams, whereas in inhabited by brown trout. However, considering the direction and North America these same streams are the ultimate refuge area for ECOLOGY rate of brook trout expansion, it is likely that brook trout will soon brook trout under the invasion pressure by brown trout. Thus, invade these streams, eventually replacing the native species, which comparing the species’ fundamental niches provides the basis for understanding the seemingly inconsistent pattern of species replacement during invasion on each continent. Importantly, this result implies that if the niche characteristics of an introduced organism are well known, its invasion potential in an area can be predicted and management actions can be targeted accordingly (2). The reciprocal pattern of invasion demonstrated here under- lines the vital importance of autecological information in both native and nonnative ranges for explaining and predicting invasions (see ref. 22). For the widely studied and commercially important salmonid fishes such information is largely available, but there are numerous other instances where even the key ecological traits and niche requirements of the species involved are insufficiently known, making invasions often look entirely unpredictable (23). A combination of carefully designed exper- iments and long-term monitoring of both the invading and the native species are therefore needed to clarify the population- level mechanisms underlying the idiosyncratic and sometimes even paradoxical patterns of invasion (24, 25). Genetic stocks of brown trout are considered threatened in many parts of Europe (26, 27). Therefore, the few naturally reproducing populations that still remain in headwater streams have high adaptive and evolutionary significance and, therefore, high conservation value for the species whose populations in lowland rivers are affected by extensive aquaculture releases (28). Ironically, headwaters are the very environment where brown trout is most likely to be replaced by its alien competitor, brook trout. Furthermore, headwater streams comprise a unique biodiversity resource, supporting a number of freshwater taxa absent from larger rivers (29, 30). They have a long history of human exploitation and are therefore considered seriously threatened all over the world (31, 32). Although habitat degra- dation is the primary cause for changes to headwater ecosystems, invasions by exotic species may add to further loss of biodiversity in these endangered habitats. We therefore strongly urge that Fig. 3. Proportion of study sites (%) in small (Ͻ7 m wide, A) and large (Ͼ7 m, B) streams that supported age-0 brown trout. ■, brook trout present in any further stocking of brook trout and other nonnative salmo- both years (small streams, n ϭ 11; large streams, n ϭ 5); ᮀ, brook trout invasion nids to North European streams be strictly regulated or, rather, sites (n ϭ 5 and 15, respectively); ϫ, allopatric brown trout sites (n ϭ 6 and 20). ceased altogether.

Korsu et al. PNAS ͉ June 5, 2007 ͉ vol. 104 ͉ no. 23 ͉ 9727 Downloaded by guest on September 27, 2021 Materials and Methods (36). Altogether 762 brook trout and 1,270 brown trout were Study Area. The study area comprises the upper parts of the River sampled during the two study years. Kemijoki drainage system, northeastern Finland (between In 2004 we measured several habitat variables at each site. 67°15ЈN and 68°00ЈN; 28°00ЈE and 29°10ЈE) (see SI Fig. 4). Measurements were made along randomly placed cross-sectional Although the lower parts of the river hold several dams, only one transects covering the whole study section. The number of mea- is located within our study area, blocking the upstream migration surements varied between 18 and 25, depending on stream width. into one of the 69 study sites. The virtual absence of lakes in the At each site we assessed the percent cover of instream vegetation drainage system results in high snowmelt-induced floods in May. (mainly bryophytes), canopy shading (percentage of cover), and The main stream is meso-to-oligotrophic [mean and range of dominant substrate size (modified Wentworth scale) (see SI Table total phosphorus in 1973–2004: 15 (2–57) ␮g⅐literϪ1] and cir- 2), and we measured current velocity (at 0.6 ϫ depth with Schilt- cumneutral (mean pH 6.9, range 6.0–7.8) (Archives of the knecht MiniAir 20), water depth, and stream width. We also Regional Environmental Centre of Lapland, Finland). Smaller measured pH and conductivity (␮S⅐cmϪ1) for each site using a tributaries tend to be more acid with pH minimum Ͻ5. portable recorder (pH/Cond 340i; Wissenschaftlich-Technische The study sites are mainly low-gradient (mean slope 0.7 Werksta¨tten,Weilheim, Germany). m⅐kmϪ1) streams, with a pool-riffle sequence characteristic of unmodified forest streams. The sites are scattered across the Data Analysis. We divided the sampling sites into four categories Upper Kemijoki River drainage system, comprising variable based on the presence or absence of the two trout species stream habitats from wide, open channels to narrow, heavily (allopatric brook trout sites, sympatric sites, brook trout invasion shaded headwater streams (SI Table 2). Although most of the sites, and allopatric brown trout sites) (see Table 1). To dem- study sites are historically impacted by forestry, they have onstrate possible species replacement, we calculated brown remained practically untouched for at least 40 years and are trout/brook trout density ratios (percentages) for each site, with therefore nearly pristine. Salmonid populations in the study area 100 indicating complete domination by brown trout and 0 are mainly resident, and fishing pressure is negligible. Therefore, indicating complete domination by brook trout. Absolute den- at present, the only potential human-induced threat to stream sities were not used because they were highly variable (0.004– integrity in the system is the introduction of the alien fish species 0.79 individuals per m2), potentially masking any system-wide brook trout. effects of brook trout on brown trout. To compare trout densities Brown trout is the only native trout species in the study system, between time periods and site categories we used two-way comprising 18% of total fish density. Other native species, in repeated measures ANOVA. Seven sites where brook trout order of abundance, are bullhead, European minnow (Phoxinus occurred in 1994 but not in 2004 were omitted from the analysis. phoxinus L.), Alpine bullhead (Cottus poecilopus Heckel), brook We used a paired t test to test for density ratio changes in lamprey (Lampetra planeri Bloch), burbot (Lota lota L.), nine- sympatric assemblages. To examine the effect of brook trout on spined stickleback (Pungitus pungitus L.), and European grayling the reproduction of brown trout, we calculated the number of (Thymallus thymallus L.). The mean number of fish species per sites where age-0 brown trout were found, separately for small study site was three in both years (range 1–7). (Ͻ7 m) and large (Ͼ7 m) streams in each of three site categories: More than 1.5 million mainly age-0 brook trout were intro- (i) sites where brook trout were present in both years, (ii) invaded duced in the middle and southern parts of the study area between sites (brook trout present in 2004 but not 1994), and (iii) 1972 and 1978 (Archives of the Finnish Game and Fisheries allopatric brown trout sites (brook trout absent in both years). Research Institute). Stocking ceased in 1983, and the only fish Principal component analysis (PCA) was used to examine fish– stocked ever since has been brown trout (annual mean of 14,000 habitat relations. Environmental variables were log- or arcsin- individuals, age 1–5 years). Brook trout now constitutes 15% of transformed, if needed, to better meet the assumptions of PCA. The the total fish density in the drainage system, and its average analysis produced four components with eigenvalues Ͼ1.0 (SI density is comparable to that of brown trout. Table 2). We then performed one-way ANOVA followed by Tukey’s pairwise comparisons for each component to examine Sampling Protocol. The first electrofishing survey was conducted by whether site categories, represented by site scores in PCA, differed the Finnish Game and Fisheries Research Institute in 1993 and in stream habitat structure. We performed all statistical analyses 1994 (referred here as the 1994 sampling) during the late-summer with SPSS for Windows version 12.0.1 (SPSS, Chicago, IL). low-flow conditions (33). In August 2004 we revisited the same sites (n ϭ 69 in 32 streams, mean sample area 289 m2) and collected fish We are indebted to Pekka Korhonen for collecting the 1994 data set. using exactly the same methods as in the previous survey. Fish Tapio Rautiainen and Olli van der Meer led the groups of highly densities were estimated by the removal method (34, 35). All motivated field workers, which made possible the collection of the 2004 captured fish were measured, identified, and returned to the stream. data set within a reasonable time period. We also appreciate comments Age-0 (young-of-the-year) fish were separated from the older ones by two anonymous referees on a previous version of the manuscript. based on scale analysis and length-frequency histograms. We Financial support was provided by the Maj and Tor Nessling Foundation consider the presence of age-0 fish to indicate local reproduction and the Academy of Finland.

1. Mack RN, Simberloff D, Lonsdale ML, Evans H, Clout M, Bazzaz FA (2000) 14. Holcˇik J (1991) Can J Fish Aquat Sci 48(Suppl 1):13–23. Ecol Appl 10:689–710. 15. Strauss SY, Webb CO, Salamin N (2006) Proc Natl Acad Sci USA 103:5841– 2. Peterson AT, Vieglais DA (2001) BioScience 51:363–371. 5845. 3. Kolar CS, Lodge DM (2002) Science 298:1233–1236. 16. Stoneman CL, Jones ML (2000) Trans Am Fish Soc 129:639–657. 4. Moyle PB, Marchetti MP (2006) BioScience 56:515–524. 17. Rahel FJ, Nibbelink NP (1999) Can J Fish Aquat Sci 56(Suppl 1):43–51. 5. Moyle PB, Light T (1996) Biol Conservation 78:149–161. 18. Baldigo BP, Lawrence GB (2000) Trans Am Fish Soc 129:60–76. 6. Elliott JM (1989) Freshwater Biol 21:1–5. 19. Pirhalla DE (2004) Trans Am Fish Soc 133:144–159. 7. Krueger CC, May B (1991) Can J Fish Aquat Sci 48(Suppl 1):66–77. 20. Schlosser IJ, Ebel KK (1989) Ecol Monogr 59:41–57. 8. Fausch KD, White RJ (1981) Can J Fish Aquat Sci 38:1220–1227. 21. Flebbe PA (1994) Trans Am Fish Soc 123:657–667. 9. DeWald L, Wilzbach MA (1992) Trans Am Fish Soc 121:287–296. 22. Hierro JL, Maron JL, Callaway RM (2005) J Ecol 93:5–15. 10. Waters TF (1999) Trans Am Fish Soc 128:1151–1162. 23. Lodge DM (1993) Trends Ecol Evol 8:133–137. 11. Townsend CR (2003) Conservation Biol 17:38–47. 24. Sax DF, Brown JH (2000) Global Ecol Biogeogr 9:363–371. 12. Morita K, Tsuboi J-I, Matsuda H (2004) J Appl Ecol 41:962–972. 25. Peterson DG, Fausch KD (2003) Biol Invas 5:239–259. 13. Vooren CM (1972) J Fish Biol 4:565–583. 26. Almodo´var A, Nicola GG (2004) Fish Manage Ecol 11:173–184.

9728 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0610719104 Korsu et al. Downloaded by guest on September 27, 2021 27. Rassi P, Alanen A, Kanerva T, Mannerkoski I, eds (2001) The Red List of 31. Benke AC (1990) J N Am Benthol Soc 9:77–88. Finnish Species (Ministry of the Environment and Finnish Environment Inst) 32. Malmquist B, Rundle S (2002) Environ Conservation 29:134–153. (Finnish with English summary). 33. Korhonen P, Koskiniemi J, Tolonen K (1996) Kalatutkimuksia: Fiskunderso¨kn- 28. Northcote TG (1997) N Am J Fish Manage 17:1029–1045. ingar 106 (Finnish Game and Fisheries Research Inst) (Finnish with English 29. Furse MT (2000) in Assessing the Biological Quality of Fresh Waters, eds Wright summary). DW, Sutcliffe WD, Furse MT (Freshwater Biol Assoc, Ambelside, UK), pp 34. Bohlin T, Hamrin S, Heggberget TG, Rasmussen G, Saltveit SJ (1989) 79–92. Hydrobiologia 173:9–43. 30. Heino J, Muotka T, Mykra¨H, Paavola R, Ha¨ma¨la¨inen H, Koskenniemi E 35. Carle FL, Strub MR (1978) Biometrics 34:621–630. (2003) Ecol Appl 13:842–852. 36. Beard TD, Carline RF (1991) Trans Am Fish Soc 120:711–722. ECOLOGY

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