Ecological and Life History Characteristics of Ruffe (Gymnocephalus Cernuus) in Relation to Other Freshwater Fish Species

J. Great Lakes Res. 24(2):228-234 Internat. Assoc. Great Lakes Res., 1998

Ecological and Life History Characteristics of Ruffe (Gymnocephalus cernuus) in Relation to Other Freshwater Fish Species

Jyrki Lappalainen* and Jakob Kjellman Department of Limnology and Environmental Protection P.O. Box 27, FIN-00014 University of Helsinki, Finland

ABSTRACT. Ecological and life history characteristics of ruffe (Gymnocephalus cernuus) were studied in relation to 33 other native freshwater fish species in Finland. The descriptive ecological characteristics included 1) trophic guild, 2) species interaction, 3) adult habitat, 4) spawning habitat, 5) reproductive behavior, and 6) reproductive guild. The life history variables included 1) age at maturity, 2) length at maturity, and 3) fecundity as a number of eggs. Three different clusters of fish species were found in cluster analysis based on the ecological characteristics. The most distinct cluster of 7 species was comprised of predators. Ruffe was grouped into the largest cluster together with 20 other species and was closest to the cyprinid, gudgeon (Gobio gobio). In multidimensional scaling species were placed in two hypothetical dimensions firstly by their interaction with other species, trophic guild and adult habitat and secondly by their spawning habitat. Ruffe was placed near the center of the plot, suggesting that it has no special ecological requirement among the characteristics and species studied. Subsequent analysis of the life history characteristics revealed that ruffe was similar to the most typical r-selected species in Finland, showing high fecundity and low length at maturity, but with slightly slower growth rate. We, therefore, concluded that adult ruffe is a potential invader species showing no special ecological requirements and with life history characteristics typical for r-selected species.

INDEX WORDS: Ruffe, life history, ecological characteristics, Finland, r-selected.

INTRODUCTION Ruffe (Gymnocephalus cernuus) is a common benthic fish species in Finnish freshwaters. Other frequently occurring species in addition to ruffe include Eurasian perch (Perca fluviatilis), northern pike (Esox lucius), roach (Rutilus rutilus), and burbot (Lota lota) (Koli 1981, Tonn et al. 1990). As with many other small-sized fish, ruffe has received little attention due to its low economic value. However, in recent years it has colonized new waters outside its former distribution range. In these newly colonized waters the abundance of ruffe has increased to high levels, a circumstance that has raised questions concerning its possible negative effects on indigenous fish species (e.g., Pratt et al. 1992, Rösch and Schmid 1996, Savino and Kolar 1996, Winfield et al 1996). The purpose of the present paper was to examine the ecological similarities of ruffe in relation to other native freshwater fish species in Finland, based on six ecological characteristics. We were interested in how various species are placed in hypothetical dimensions and especially in relation to ruffe, based on these six ecological characteristics. We hypothesised that species near each other, thus showing similarities in the ecological characteristics examined, should compete for niche dimensions when co-occurring.

*Corresponding author. E-mail: [email protected] The species studied were also classified according to their age, fecundity, and length at maturity. Mandrak (1989) has shown that successful invaders have broad niche dimensions and life history characteristics typical for r-selected species. In general, r-selected species have short generation time, small size, high fecundity, and rapid growth. Hence we sugges- ted that ruffe should be closer to r-selected than K-selected species among the native freshwater fish species in Finland.

MATERIALS AND METHODS

Ecological and Life History Characteristics

Ecological and life history characteristics were estimated for the 34 freshwater fish species native to Finland. This classification was based mostly on Finnish literature (Pitkänen 1961; Seppovaara 1982; Koli 1984, 1990; Mikelsaar 1984; Kangur and Kangur 1996). Ecological characteristics were estimated for adult fish at an age corresponding to maturity in about 50% of the fish and included 1) trophic guild, 2) species interaction, 3) adult habitat, 4) spawning habitat, 5) reproductive behavior, and 6) reproductive guild. These characteristics were the same as those used by Mandrak (1989) with the exception that the adult and spawning habitats were further divided into lentic and lotic water habitats and the reproductive guild was classified in more detail. The trophic guild was determined by the type of adult food comprising at least 75% of the diet. The categories were herbivory, planktivory, insectivory, piscivory, and omnivory. Species interactions were classified into three categories: predator, prey, or neither. Further, the adult and spawning habitats were characte- rized as lentic and lotic waters by the type of depth continuum: wetland, nearshore, benthic, and pelagic. Reproductive behavior and guild were classified according to Balon (1975). Thus species were classified based on their reproductive behavior as nonguarders or guarders. The nonguarders included open-substrate spawners or brood hiders, and the guarders were substrate choosers, nest builders, or internal bearers. Based on the reproductive guild, species were either litho-pelagophils, lithophils, phyto-lithophils, phytophils, psammophils, speleophils, or ariadnophils. All three life history characteristics of age, fecundity, and length were classified according to the age corresponding to maturity in about 50% of the fish. Fecundity, as the number of eggs, was divided into five classes based on a logarithmic scale: 1) 1 to 100, 2) 101 to 1,000, 3) 1,001 to 10,000, 4) 10,001 to 100,000 and 5) 100,001 to 1,000,000. The length at maturity (cm) was classified into the following groups: 1) 1 to 10, 2) 11 to 20, 3) 21 to 40, 4) 41 to 80, and 5) > 80. The ecological and life history characteristics of the species studied were analyzed inde- pendently of their possible occurrence in lakes. Species having many ecological forms such as whitefish (Coregonus lavaretus) and brown trout (Salmo trutta) characteristics typical of lake forms were included. The characteristics thus used for whitefish were of the form having a mean of 42 gillrakers, while those for brown trout were typical of Salmo trutta m. lacustris.

Statistical Analysis Cluster analysis (SYSTAT 1992) was used to classify the freshwater fish species according to their ecological characteristics. Since these characteristics were categorical, cluster analysis was based on disagreement percentage among the species. Thus, if all six characteristics were the same, the disagreement percentage would be 0%, as noted for three-spined stickleback (Gasterosteus aculeatus) and nine-spined stickleback (Pungitius pungitius). On the other hand, if no categorical characteristics were the same, the disagreement percentage would be 100%, as noted for ruffe and Arctic char (Salvelinus alpinus). Multidimensional scaling was also based on disagreement percentages scaled between 1 and 0. Species were partitioned into clusters with K-means clustering based on their life history characteristics (SYSTAT 1992). The clustering was started with three partitionings, because we expected that at least three groups of species could be found showing characteristics typical for either r- or K-selected species or falling between these two limits. Preliminary analysis showed that four clusters with only one or two species were already formed with six partitions and the results were difficult to interpret. Therefore, no further partitionings were analysed.

RESULTS

Ecological Characteristics Cluster analysis formed three large groups of species based on ecological characteristics (Fig. 1). All seven predators were grouped into cluster I. Ruffe was grouped into the largest cluster with 20 other fish species. The species in this cluster were all open-substrate spawners except the three- and nine-spined sticklebacks. Cluster II could be further divided into three smaller clusters based on trophic guild. All species in cluster IIa were plankti- vorous, in cluster IIb insectivorous except rudd (Scardinius erythrophthalmus), and species in cluster IIc were omnivorous. In cluster IIb ruffe was grouped into the same cluster with a cyprinid gudgeon (Gobio gobio). Four of the ecological characteristics studied were the same for ruffe and gudgeon: trophic guild, species interaction, spawning habitat, and reproductive behavior (Appendix).

The fish species studied were ordinated based on interaction with other species, trophic guild, adult, and spawning habitats in two hypothetical dimensions in multidimensional scaling (Fig. 2). In dimension 1 species were placed by their interaction with other species and trophic guild. Predators, i.e., piscivorous species, were placed on the left side of the plot, while nonpiscivorous species were placed on the right side. Furthermore, dimension 1 indi- cated changes in adult habitat from pelagic on the left to benthic and nearshore habitats on the right side of the plot. In dimension 2 species were scaled by their spawning habitat. In the upper part of the graph were lentic-wetland or nearshore spawners, while in the lower part of the plot the species were mainly benthic spawners.

Ruffe was placed near the center of the plot in multidimensional scaling (Fig. 2). Subsequent scaling with only the species in cluster II showed, once again, that ruffe was placed near the center, suggesting that ruffe has no special requirements among the species and ecological characteristics studied.

Life History Characteristics All life history characteristics were correlated with each other (Fig. 3). The strongest corre- lation (Spearman) was found between age and length at maturity (rs = 0.73, P < 0.01, n = 34), but correlations between fecundity and length (rs = 0.60, P < 0.01, n = 34) and fecundity and age (rs = 0.52, P < 0.01, n = 34) were also significant.

In K-means clustering ruffe was always grouped into the same cluster despite the number of partitions based on life history characteristics. Other species in this group included vendace (Coregonus albula), smelt (Osmerus eperlanus), gudgeon, bleak (Alburnus alburnus), silver bream (Blicca bjoerkna), Crucian carp (Carassius carassius), stone loach (Noemacheilus barbatulus), spined loach (Cobitis taenia), three-spined stickleback, nine-spined stickleback, bullhead (Cottus gobio), Alpine bullhead (Cottus poecilopus), and fourhorned sculpin (Myoxocephalus quadricornis). These species appeared to be rather r-selective with low age at maturity (minimum and maximum of the mean in 3 to 6 partitionings = 2.43 to 2.71 years) and high fecundity (2.88 to 2.98) in relation to length at maturity (1.47 to 1.53). When compared with other species in this group ruffe showed higher fecundity (class 3, e.g., 1,001 to 10,000 eggs) and age at maturity (3 years), but slower growth (length at maturity class 1, e.g., < 10 cm).

DISCUSSION Ruffe is among the shortest species to attain maturity in Finland (Fig. 3). It is already mature at lengths under 10 cm and at 2 to 3 years of age (Koli 1990). Age at maturity appears to be a compensation for slow growth rate and high mortality (Lind 1977). One notable aspect is that none of the species studied was mature at age 1, which is probably due to their northern location in Finland. Most of the species studied occur near the northern limits of their distribution ranges; only 11 species are found throughout Finland (Koli 1990). In multidimensional scaling ruffe was placed rather far from other common freshwater fish species in Finland, namely Eurasian perch, northern pike, roach, and burbot (Fig. 2) (Koli 1981, Tonn et al. 1990). However, roach, perch, and pike were scaled near each other, suggesting possible competition. Bergman (1990) has shown that increased density of roach caused decreased growth of both perch and roach, but no significant growth decrease was observed for ruffe. Although ruffe show lower maximal foraging ability compared with perch, it compensates for this by being more tolerant to spatial and temporal variations in light and temperature (Bergman 1987, 1988). These two environmental factors could, therefore, mediate the coexistence of ruffe and perch in the same waters (Bergman 1990). Species placed near each other and at the same time far from the center in multidimensional scaling may also compete for niche dimensions. Based on literature this appears to be the case, e.g., when the two bullheads occur in the same lakes or rivers, usually bullhead dominates over Alpine bullhead (Andreasson 1969, Koli 1990). Furthermore three-and nine- spined sticklebacks occur only in the same lakes in northern Finland (Koli 1981). The predators salmon (Salmo salar), brown trout, and Arctic char also show different habitat preferences, e.g., in spawning (Koli 1984, 1990). The only cyprinid predator in Finland, asp (Aspi- us aspius), prefers lotic habitats, whereas pikeperch (Stizostedion lucioperca) prefers large lakes (Lind 1977, Koli 1984, Lehtonen et al. 1984). The causes of rapid colonization by ruffe are not known or may vary among different water systems. In general, several human-based stresses such as eutrophication are involved (Hansson 1985, Bergman 1991). In a summary of a study by Regier and Henderson (1973), Walters (1986) pointed out five typical changes in disturbed ecosystems: 1) spatial heterogeneity and species diversity are reduced, 2) temporal variability is increased, 3) overall body size distribution is reduced toward smaller forms and species that turn over more rapidly and erratically, 4) stress shifts energy and nutrient flows maintenance pathways into net-output pathways, and 5) the harvesting of valuable species causes stress, which favors species of lesser value. Most of these changes appear to benefit ruffe, as it is known to withstand increased temporal variability better than species having special ecological requirements (e.g., Bergman 1987, 1988; Rosch et al. 1996). Since it is a small, r-selected species, ruffe can utilize these new energy pathways more efficiently. In addition, the fishing of more valuable species should further benefit ruffe, which is of low economic value. According to a review by Ross (1986), the most important factors affecting niche dimensions in fish assemblages are diet and habitat axis, and to a lesser extent temporal or other abiotic factors. These findings are in accordance with our results. An obvious weakness in our analysis is that no ecological characteristics for larval or juvenile phases were studied. A more complete picture of the niche dimension could, therefore, be obtained by including more detailed data on the ecological characteristics for both adult and juvenile fishes (e.g., Ross 1986, Bergman and Greenberg 1994). Moreover, we are aware that factors such as microhabitat preferences and nondirect effects through food webs can affect niche dimensions (e.g., Mills and Forney 1988, Horppila and Kairesalo 1992, Erkinaro 1997). Our results, however, showed that adult ruffe is a potential invader and r-selected species having no special ecological requirements.

ACKNOWLEDGMENTS This study was funded by the Emil Aaltonen Foundation (J.L.) and the 350th Anniversary Foundation of the University of Helsinki (J.K.). We thank the three reviewers for their com- ments.