J. Great Lakes Res. 24(2): 170-1 85 Internat. Assoc. Great Lakes Res., 1998

A Synopsis of the Biology and Life History of Ruffe

Derek H. Ogle* Northland College Mathematics Department Ashland, Wisconsin 54806

ABSTRACT. The ruffe (Gymnocephalus cernuus), a Percid native to Europe and Asia, has recently been introduced in North America and new areas of Europe. A synopsis of the biology and life history of ruffe suggests a great deal of variability exists in these traits. Morphological characters vary across large geographical scales, within certain water bodies, and between sexes. Ruffe can tolerate a wide variety of conditions including fresh and brackish waters, lacustrine and lotic systems, depths of 0.25 to 85 m, montane and submontane areas, and oligotrophic to eutrophic waters. Age and size at maturity dif- fer according to temperature and levels of mortality. Ruffe spawn on a variety ofsubstrates, for extended periods of time. In some populations, individual ruffe may spawn more than once per year. Growth of ruffe is affected by sex, morphotype, water type, intraspecific density, and food supply. Ruffe feed on a wide variety of foods, although adult ruffe feed predominantly on chironomid larvae. Interactions (i.e., competition and predation) with other species appear to vary considerably between system. INDEX WORDS: Ruffe, review, taxonomy, reproduction, diet, parasite, predation.

INTRODUCTION DISTRIBUTION This is a review of the existing literature on Ruffe are native to all of Europe except for along ruffe, providing a synopsis of its biology and life the Mediterranean Sea, western France, Spain, Por- history. A review of the existing literature is tugal, Norway, northern Finland, Ireland, and Scot- needed at this time because the ruffe, which is na- land (Collette and Banarescu 1977, Lelek 1987). In tive to Europe and Asia, has recently been intro- Asia, ruffe are native only in Siberia, but not the duced in North America and new areas of Europe. Amur River or Transcaucasia (Berg 1949). Furthermore, Rosch et al. (1996) suggested that “a Ruffe were accidentally introduced to several synopsis of this species is desirable and should be areas in the late 1980s and early 1990s. Ruffe are attempted.” Currently available synopses of ruffe now found in Loch Lomond, Scotland (Maitland et are incomplete (Rosch et al. 1996), in the gray lit- al. 1983); Llyn Tegid, Wales (Winfield 1992); erature (Ogle 1995), or geographically restricted Bassenthwaite Lake, England (Winfield 1992); (see other reviews in this volume). In this paper the Lake Constance, Germany (Rosch and Schmid published information, which was available prior 1996); Lake Mildevatn, Norway (Kalas 1995); the to the convening of this symposium, will be re- Camargue region, France (E. Rosecchi, Station Bi- viewed. The paper will focus on the distribution, ologique de la Tour du Valat, pers. comm.); Italy taxonomy and nomenclature, evolution and genet- (Chiara 1986); Lake Superior, United States (Simon ics, sensory physiology, habitat, reproduction and and Vondruska 1991, Pratt et al. 1992); and Lake early life history, age and growth, diet and foraging behavior, competitors, predators, parasites and Huron, United States (T. Busiahn, U.S. Fish and pathology, and possible methods for control of Wildlife Serv., pers. comm.). ruffe populations. TAXONOMY AND NOMENCLATURE The accepted name for ruffe is Gymnocephalus cernuus (American Fisheries Society I99 1, Rosch et al. 1996). Linnaeus introduced the species as *Corresponding author E-mail dogle@wheeler northland edu Perca cernua in 1758. More recently the ruffe has

170 Biology and Life History of Ruffe 171

TABLE 1. Summary of meristics for European and Asian ruffe. Character Range Character Range Dorsal 10-15 Lateral-line scales 33-42 Anal II-III 4-7 Scales below lateral line 10-18 Pectoral 13-17 Scales above lateral line 5-10 Opercular spines I Branchiostegal rays 6-7 Preopercular spines 7-16 Gill rakers, first arch 6-14 Vertebrae 31-36 been named Acerina cernua and G. cernua (Col- specific morphological aspects have been described lette 1963). Ruffe have various local common in great detail: the ctenoid scales (Coburn and names including jezdik (former Czechoslovakia), Gaglione 1992); the cephalic skeletal and muscular horke (Denmark), stone-perch or pope (England), systems (Elshoud-Odenhave and Osse 1976); the kiiski or kueski (Finland), perche goujonniere or cephalic lateral line system (Jakubowski 1967, Brenilie (France), kaulbarsch (Germany), kulbaars Disler and Smirnov 1977); the eye and optical sys- (Netherlands), nork or steinpurke (Norway), jazgarz tem (Sroczynski 1981); and the relationship be- (Poland), ghibort (Romania), ersh or jorsch (Rus- tween total length and the size of several body parts sia), gers (Sweden), and iorzh or bubyr’ (Ukraine). (Matkovskiy 1987, Nedelkova and Zaveta 199 1). The ruffe is a member of the Percidae. Subfamily Morphological differences may exist on several nomenclature differs among authors. Collette geographical scales and between sexes. Witkowski (1963) and Collette and Banarescu (1977) placed and Kolacz (1 990) suggested that body depth, pre- ruffe in the tribe Percini with Perca and Percarina. dorsal distance, preanal distance, first dorsal depth, The tribes Percini and Etheostomatini make up the anal fin length and depth, and pectoral length gen- subfamily Percinae. Wiley (1 992) proposed two erally declined from east (Europe) to west (Siberia). subfamilies, Percinae and Etheostomatinae. Only Differences in body shape of ruffe within a water- Perca is in the Percinae and Gymnocephalus are the shed have also been described (Aleksandrova 1974, basal taxon for the Etheostomatinae. The subfamily Nedelkova and Zaveta 199 1 ). Sexual dimorphism nomenclature of Page (1985) and Coburn and has been observed for some characteristics (e.g., Gaglione ( 1992) depended largely on their belief eye diameter; preventral, prepectoral, and anal- that ruffe produce egg-strands, for which no evi- caudal distances; head length; and body thickness, dence could be found in the literature. summarized by Aleksandrova 1974). Four species of Gymnocephalus have been de- scribed, G. schraetser, G. acerina, G. baloni, and EVOLUTION AND GENETICS G. cernuus. Characteristics synapomorphic for All known Gymnocephalus fossils are G. cernuus Gymnocephalus are enlarged preopercular spines, a from interglacial deposits in Denmark, Germany, small (< 1 cm) anterior to ventral ramus ratio, a England, Poland, and Russia (Holcik and Hensel club-like distal end of the premaxilla, a retroarticu- 1974). The basal Gymnocephalus species may be G. lar that is distinctly higher than long when viewed cernuus, as G. acerina and G. schraetser appear medially (Wiley 1992), and hypertrophy of the more “primitive” and G. baloni apparently recently cephalic lateral-line canals (Collette and Banarescu derived from G. cernuus (Holcik and Hensel 1974). 1977). Holcik and Hensel (1974) suggested two Gymnocephalus cernuus is apparently of Paleo- subgenera, Gymnocephalus and Acerina, based on Danube origin (Holcik and Hensel 1974, Rab et al. vertebral counts and slight color differences. Gym- 1987). nocephalus cernuus and G. baloni, with signifi- Ruffe have 2n = 48 chromosomes (Nygren et al. cantly fewer vertebrae, make up Acerina. 1968, Klinkhardt 1990). The types of chromosome General morphological descriptions were made pairs differ among studies. Bozhko et al. (1980) by Collette ( 1963), Aleksandrova (1 974), Holcik found 2 metacentric, 11 submetacentric, 8 subelo- and Hensel (1\974), Collette and Banarescu (1977), centric, and 3 acrocentric; Rab et al. (1987) found 1 Matkovskiy ( 1987), Nedelkova and Zaveta ( 199 1 ), metacentric, I6 submetacentric, 4 subelocentric, and Wiley (1 992). Selected meristics from these and 3 acrocentric; and Mayr et al. (1987) found studies are summarized in Table I. The following only I acrocentric. Nyman (1969) and Logvinenko 172 Derek H. Ogle et al. ( 1983) described polymorphic serum esterases with the bottom (Holcik and Mihalik 1968, Sand- that could be used in population investigations. The lund et al. 1985, Bergman 1988); and 3) ruffe in- karyotypes of the four Gymnocephalus species are crease in abundance with increasing eutrophication. unique (Rab et al. 1987). Ruffe can hybridize with The abundance of ruffe increases with eutrophi- Perca fluviatilis (Kammerer 1907, as cited in cation until hypereutrophy is reached (Entz 1977, Hokanson 1977) and G. baloni (Holcik and Hensel Leach et al. 1977, Hansson 1985, Johansson and 1974). Other aspects of the genetics of ruffe were Persson 1986, Bergman 199 1, Persson et al. 199 1 ). described recently by Rosch et al. (1996). Bergman (1991) showed that the abundance of ruffe generally increased in lakes ordered along a pro- SENSORY PHYSIOLOGY ductivity gradient. Ruffe abundance increased with anthropogenic additions of nutrients in several situ- Ruffe have an extremely sensitive cephalic lat- ations (Heinonen and Falck 1971, Anttila 1973, eral-line system with 25 cupulae embedded in bony Hansson 1987, Neuman and Karas 1988). In con- canals covered with a stretched-skin membrane trast, Leopold et al. (1 986) found no correlation be- (Jakubowski 1967). The bony canals afford protec- tween level of eutrophication and ruffe catch tion to the neuromasts. High sensitivity is main- because of high year-to-year variability in catches. tained by a large number of nerve fibers per In other cases, ruffe abundance declined with in- neuromast and receptors per nerve fiber (Gray and creasing eutrophication (Biro 1977) or ruffe abun- Best 1989), the large size of the canals (Denton and dance increased after major nutrient additions were Gray 1988), and the membrane (Denton and Gray eliminated (Peirson et al. 1986). 1988). The ultrastructure and electrical physiology Four possible hypotheses may explain the posi- of this system has been actively studied (Flock tive relationship between eutrophication and abun- 1967, Kuiper 1967, Disler and Smirnov 1977, Gray dance of ruffe. First, ruffe forage more efficiently and Best 1989, Denton and Gray 1989, Van Netten under reduced light conditions associated with in- 1991, Wubbels 1991). Disler and Smirnov (1977) creased algal production (Johansson and Persson described the development of the system during the 1986; Bergman 1988, 1991). Second, benthos may early life history period. increase in abundance and diversity and shift to Ruffe possess a tapetum lucidum in the dorsal smaller species in response to the storage of in- two-thirds of the pigmented epithelial layer of the creased energy in the sediment due to eutrophica- retina (Ahlbert 1970, Craig 1987). The tapetum lu- tion (Leach et al. 1977). Benthic-feeding ruffe cidum aids vision in low-light conditions because it might be favored by the increased production and reflects light for additional absorption by the rods shift to smaller species. Third, increased productiv- (Zyznar and Ali 1975, Ali et al. 1977). In addition, ity may release predation pressure on ruffe the photoreceptors of ruffe are arranged in an irreg- (Bergman 1991). Fourth, ruffe may be physiologi- ular twin-cone pattern that varies between row and cally more tolerant of eutrophic conditions than square configurations (Ahlbert 1970). other percids.

HABITAT REPRODUCTION AND Ruffe can tolerate a wide range of ecological and EARLY LIFE HISTORY environmental conditions (Johnsen 1965). Ruffe Ruffe commonly mature at age 2 or 3 and at total have been found in fresh and brackish (salinity to lengths near 11 to 12 cm (Lind 1977, Maitland 10 to 12 ppt) water (Lind 1977); lacustrine and lotic 1977), although maturity at age 1 has also been re- systems; depths from 0.25 m (Van Densen and Had- ported (Fedorova and Vetkasov 1974, Neja 1988). deringh 1982) to 85 m (Nilsson 1979, Sandlund et Early maturity may be a physiological response to al. 1985); montane and submontane areas warmer waters (Fedorova and Vetkasov 1974, Craig (Kawecka and Szcesny 1984), and waterbodies 1987) or a population-level response to higher mor- ranging from oligotrophic to eutrophic. Although tality rates (Lind 1977). ruffe are found in a wide variety of habitats, three Ruffe exhibit a great amount of variability in generalities about habitats used by ruffe can be spawning characteristics (e.g., habitats and condi- made: 1) ruffe prefer areas of slow-moving water tions, time of year, egg size). Spawning occurs on a with soft bottoms that are devoid of vegetation variety of substrates at depths of about 3 m or less. (Johnsen 1965, Lelek 1987); 2) ruffe are associated Balon et al. (1 977) categorized ruffe as non-guard- Biology and Life History of Ruffe 173

ing, open substrate, phytolithophil spawners that 0.45 (±0.05 SD) g and volume of 0.59 (±0.48 SD) deposit eggs on submerged plants in clean-water mm³. Eggs from the first batch are larger than eggs habitats, or on other items such as logs, branches, from the second batch (Kolomin 1977). gravel, or rocks. Maitland (1977) generally agreed Ruffe eggs hatch in 5 to 12 days at 10 to 15°C with Balon, but Collette et al. (1977) concluded (Johnsen 1965, Maitland 1977, Craig 1987, Berka that ruffe spawn on hard bottoms of sand, clay, or 1990). Newly hatched embryos of 3.5 to 4.4 mm gravel. Field evidence can be found to support both (Fedorova and Vetkasov 1974) were underdevel- conclusions (Johnsen 1965, Kovalev 1973, Fe- oped, relative to yellow perch (Perca flavescens, dorova and Vetkasov 1974, Kolomin 1977). Ruffe Disler and Smirnov 1977). The embryos remain spawn between mid-April and July at temperatures sedentary on the bottom for 3 to 7 days until reach- of 6 to 18°C (Kovalev 1973, Fedorova and ing a size of 4.5 to 5.0 mm (Disler and Smirnov Vetkasov 1974, Kolomin 1977, Willemsen 1977, 1977). The transition to exogenous feeding takes Neja 1988). Ruffe eggs develop normally at pH val- place in the benthopelagic layer (Disler and ues of 6.5 to 10.5, one of the widest ranges from a Smirnov 1977), about I week after hatching broad set of fish tested (Kiyashko and Volodin (French and Edsall 1992). Larval ruffe are posi- 1978). tively phototactic (Disler and Smirnov 1977), but Ruffe may spawn intermittently, laying two or have little or no pelagic larval stage (Johnsen 1965, more batches of eggs (Koshelev 1963, Fedorova Fedorova and Vetkasov 1974, Disler and Smirnov and Vetkasov 1974, Kolomin 1977, Neja 1988). 1977). At the larval stage, ruffe are secretive, soli- The first batch of oocytes matures in 165 days dur- tary, and do not form schools (Disler and Smirnov ing winter and spring, whereas the second batch 1977, French and Edsall 1992). Extensive details on matures in 30 days during summer (Koshelev the morphological development of ruffe embryos 1963). A mature ruffe ovary contains three types of and larvae are provided by Disler and Smirnov eggs: 1) small, hyaline, and colorless; 2) larger, (1977), Simon and Vondruska (1991), French and opaque, white or pale yellow to yellow and orange Edsall (1992), and Kovac (1994). in color; and 3) large, partly hyaline, and yellow-or- The temperature requirements of young ruffe ange and orange in color (Neja 1988). Only the lat- have been determined. The lower TL50 for em- ter two types will be released during the next bryos is 10°C and the upper TL50 is 2 1.5ºC spawning season. The physiological details of ruffe (Hokanson 1977). The optimal temperature for that spawned intermittently are given by Koshelev “early development” is 15°C (Saat and Veersalu ( 1963). 1996). Larval ruffe survival is poor below 10°C Ruffe eggs become adhesive upon contact with (Hokanson 1977). Optimal temperature for larval water, and stick to the substrate (Johnsen 1965, Ko- growth is 25 to 30°C (Hokanson 1977), whereas valev 1973). Page (1985) suggested that ruffe eggs optimal growth of age-0 ruffe occurs at 21 ºC (Ed- are extruded in “strands,” but no evidence for this sall et al. 1993). However, age-0 ruffe grew at tem- was found in any other published material. peratures between 7.0 and 24.8ºC (Edsall et al. The number of eggs deposited depends on the 1993). batch of eggs and size of the female. The number of The only detailed research concerning the repro- eggs per female is 4,000 to 200,000 for the first ductive physiology of ruffe that could be found batch (Kolomin 1977, Collette et al. 1977, Neja were those of Butskaya (1976, 1980, 1985). 1988) and 352 to 6,012 for the second batch of eggs (Kolomin 1977). Relative fecundity was 305 to 1,540 eggs per g of female (Bastl 1988, Neja 1988, AGE AND GROWTH Jamet and Desmolles 1994) and appears to be un- Female ruffe may reach age 1 I, but male ruffe correlated with body weight, gonad weight, or age generally do not exceed age 7. In most cases, fewer (Neja 1988). Average gonosomatic index was 7.1 to than six age-groups are sampled (Table 2), with 15.6 for spawning females and 7.0 to 10.0 for most fish being age 2 or younger. For example, Fe- spawning males (Kolomin 1977, Bastl 1988, Neja dorova and Vetkasov (1974) sampled seven age- 1988, Jamet and Desmolles 1994). groups with 93% of the catch being age 1 or 2. Egg diameters were 0.34 to 1.3 mm (Johnsen A firm conclusion about which calcified structure 1965, Kovalev 1973, Fedorova and Vetkasov 1974, is best for assigning age to ruffe cannot be made. Disler and Smirnov 1977, Kolomin 1977, Bastl Jamet and Desmolles (1994) found that ruffe pro- 1988). Bastl (1988) reported a mean egg weight of duced only one annulus per year on scales (in win- 174 Derek H. Ogle

TABLE 2. Total lengths-at-age (mm; except where noted) of ruffe from selected European and Asian investigations. Superscript letters following the authors ’ name and publication year indicate interpreta- tions by the following authors: A = Aleksandrova (1974), B = Boikova (1986), Ba = Bast et al. (1983), H = Holker and Hammer (1994), N = Neja (1989), and W = Willemsen (1977). Comments in the Comm. col- umn are abbreviated as follows: FL =fork length, BC = “known to be back-calculated”, f = females, m = males, sb = shallow-bodied, db = deep-bodied, fw =freshwater, br = brackish, est = estimated (from graphs or growth equation). Age Author Country I II III IV V VI VII VIII IX X Comm Adamus et al. ( 1 Poland(?) 35 55 72 84 107 125 Aleksandrova (1974) USSR 108 115 119 sb Aleksandrova ( 1974) USSR 64 96 98 109 116 db Aleksandrova ( 1974) USSR 32 64 91 104 118 sb Aleksandrova (1974) USSR 31 59 83 97 104 db Arzbach ( Germany 101 159 190 210 219 236 BC Bast et al. (1 983) Germany 97 112 132 162 BC Bast et al. (1983) Germany 80 96 112 136 169 186 BC Bast et al. (1983) Germany 126 151 176 183 BC Bauch ( Germany 60 90 1 10 120 139 Biro ( 197 I USSR 56 65 79 107 126 Fedorova & Vetkasov ( 1974) USSR 56 73 90 106 117 125 Holker & Hammer ( 1994) Germany 97 154 177 203 214 m Holker & Hammer (1994) Germany 101 157 190 207 229 241 f Johal ( 1 Czechoslovakia 66 91 107 117 132 143 151 Johal (I Czechoslovakia 64 89 106 120 136 145 157 Kijashko ( USSR 57 85 101 114 124 133 Knowles ( Germany 84 121 156 180 BC Kolander ( 1 Poland 89 106 121 137 145 161 Kolomin (1977) USSR (males) 77 113 121 125 131 141 m Kolomin (1977) USSR (females) 91 115 122 133 137 155 163 163 f Kostyuchenko USSR 38 79 I06 127 BC Kozlova (1 Russia 63 72 84 99 106 119 Lelek (1987) Europe 38 62 78 90 110 112 Lind (1977) Finland 41 73 102 118 137 143 148 167 164 fw Lind (1977) Finland I09 126 137 144 154 159 172 br Masatova and Zaveta ( Czechoslovakia 51 71 85 101 BC Neja (1988) Poland (sl) 73 106 122 137 148 158 159 157 163 m Neja (1988) Poland (sl) 72 105 122 137 148 157 162 170 172 f Neja (1988) Poland (om) 73 99 I 19 128 137 145 m Neja ( 1988) Poland (om) 74 101 119 129 43 155 164 176 179 f Neja (1988) Poland (Id) 71 99 114 128 35 143 152 m Neja (1988) Poland (Id) 72 103 122 136 43 156 169 174 f Neuhaus ( Poland 73 93 Neuhaus ( 1 Poland Noack ( Germany Nolte ( Germany br Rosch & Schmid (I 996) Germany est Sanjose ( 1984) Czechoslovakia BC Sanjose ( 1984) Czechoslovakia BC Sanjore (1984) Czechoslovakia BC Sanjose (1 984) Czechoslovakia BC Sanjose (1984) Czechoslovakia BC Shamardina ( I Russia Smirnov Russia Vasnetsov ( I Russia so Cor Biology and Life History of Ruffe 175

TABLE 2. Continued. Age Author Country IV V VI IX X Comm Vasnetsov ( Russia 37 56 89 117 136 Willemsen (1977) Netherlands 60 90 100 110 Willemsen ( Lauwersmeer 80 150 180 190 Willemsen (1977) Zalew Wislany Zbigniew ( Poland Zbigniew ( I Poland Zhukov ( 1 USSR BC Winfield et al. ( 1996) FL, est Winfield et al. (1 996) U.K. FL, est Winfield et al. ( 1996) U.K. FL, est Jamet & Desmolles (1994) France FL

ter), but Mills and Eloranta (1985) found scales to al. 1995). Age-0 ruffe larger than 3 to 5 cm gener- be inadequate for assigning age. Aleksandrova ally feed on Chironomidae (Leszczynski 1963, (1974) used otoliths as “controls” for scale-as- Nagy 1988, Ogle et al. 1995), although Boron and signed ages but did not mention any discrepancies Kuklinska (1987) described a case where mostly between the two methods. Dorsal spines (Bast et al. microcrustaceans were consumed until the ruffe 1983) and opercula (Winfield et al. 1996) have also were 5 cm long. been used. The relationships between total length The principal prey of juvenile and adult ruffe are and scale radius (Holker and Hammer 1994) and chironomids or macrocrustaceans (Table 3). The total length and otolith length (Doornbos 1979, principal genera of chironomids consumed are Chi- Matkovskiy 1987) have been developed. ronomus and Procladius (Fedorova and Vetkasov Ruffe are typically less than 20 cm in total length 1974, Boron and Kuklinska 1987, Nagy 1988, Ogle (TL), rarely exceed 25 cm TL, but may be as long et al. 1995, Kangur and Kangur 1996). The preva- as 29 cm TL (Lind 1977, Craig 1987, Lelek 1987, lence of chironomids in the diet may decrease with Berka 1990). Most of the overall length is attained increasing size or age (Leszczynski 1963, Fedorova in the first or second year of life (Table 2). Sex, and Vetkasov 1974, Ogle et al. 1995). Other mac- morphotype, water type, intraspecific density, and robenthos prevalent in the diet are Ephemeroptera, food supply affect growth of ruffe. Female, deep- Trichoptera, and Hirudinea. Ruffe collected from bodied, and freshwater ruffe grow slower than brackish or very deep waters also feed heavily on male, shallow-bodied, and brackish-water ruffe, re- macrocrustaceans such as Pallasea quadrispinosa, spectively (Table 2). A negative relationship be- Po n t opo re ia aff inis, Mys is re l i c t a , Ne o m y s is tween ruffe growth and density has been shown in integer, and Gammarus spp. (Hansson 1984, 1985; both the field (Hansson 1985) and in enclosures Sandlund et al. 1985; Van Densen 1985). Larger (Bergman and Greenberg 1994). Slow growth of ruffe eat some fish (Fedorova and Vetkasov 1974, ruffe may also result if the benthos is impoverished Kozlova and Panasenko 1977, Bagge and Hakkari (Boikova 1986, Bakanov et al. 1987) or largely in- 1985). Sierszen et al. (1996) used stable isotope accessible due to oxygen deficiencies (Boikova analyses to determine that ruffe feed on both plank- 1986). ton and benthos. Fish eggs (especially those of Coregonus spp., but also smelt (Osmerus eperlanus)) were eaten by DIET AND FORAGING BEHAVIOR ruffe in the laboratory (Mikkola et al. 1979, Ruffe first feed on rotifers and copepod nauplii Sterligova and Pavlovskiy 1984, Pavlovskiy and (Johnsen \ Larger cyclopoid copepods, clado- Sterligova 1986) and in the field (Pokrovskii I96 1, cera, and chironomid larvae are important items in Balagurova 1963, Johnsen 1965, Fedorova and the diet of age-0 ruffe larger than about 1 cm TL Vetkasov 1974, Adams and Tippett 199 I, Rosch (Johnsen 1965, Fedorova and Vetkasov 1974, and Schmid 1996). However, only one of the lab Boikova 1986, Boron and Kuklinska 1987, Ogle et studies (Pavlovskiy and Sterligova 1986) offered an 176 Derek H. Ogle

TABLE 3. Major food items of ruffe from Johnsen’s (1965) review and from selected other investiga- tions. Superscript letters following the authors’ name and publication year indicate interpretations by the following authors: B = Bergman (1987), Bo = Boikova (1986), BK = Boron and Kuklinska (1987), J = Johansson and Persson (1986), and N = Nagy (1988). Author Country Major Food Items from Johnsen (I965) Alm (1917) Sweden Chironomidae, Alona, Cyclopoida Alm ( 1922) Sweden Chironomidae, Asellus Brofeldt ( 1922) Germany Asellus, Chironomidae, Entomostracha Hartley ( 1940) England Chironomidae, Crustacea Huitfeldt-Kaas (19 17) Norway Pallasea, Mys is, Chironomidae Jaaskelainen ( I9 I 7) USSR Chironomidae, Pisidium, Insecta larvae Jarnefelt ( 19 17) Finland Asellus, Trichoptera, Cladocera Jarnefelt (1921) Finland Asellus, Ephemeroptera, Chironomidae Kessler (1 868) USSR Gummarus, Mysis, Pontoporeia Leszczynski (1963) Poland Chironomidae Levander ( 1909) Finland Chironomidae, Gammarus, Couophiunz Mohr ( 1923) Germany Gummarus, Tubifex, Mysis Neuhaus ( 1934) Germany Asellus, Chironomidae, Corophium Schneider (1922) Finland Chironomidae, Trichoptera, Cyclopoida Schneider ( 1922) Estonia Chironomidae, Trichoptera, Asellus, Cladocera Schneider ( 1922) Estonia Chironomidae, Limnophilidae, Entomostracha Stadel ( 1936) Germany Gammarus, Copepoda Tolg ( 1960) Hungary Chironomidae, Cyclopoida, Corophium Other Authors Adams & Tippett ( 199 1) Scotland Whitefish eggs, Trichoptera, Crustacea Aleksandrova (1 974) USSR Chironomidae, Gummarus, Oligochaeta Appelberg ( 1990) Sweden Chironomidae, Asellus Bagge and Hakkari ( 1985) Finland Chironomidae, Mysis, Pallasea Bergman ( 1990) Sweden Chironomidae, Ephemeroptera, Crustacea Bergman ( 199 I ) Sweden Chironomidae, Ephemeroptera, Crustacea Bergman & Greenberg ( 1994) Sweden Sialis, Chironomidae, Ephemeroptera, Trichoptera Berka ( 1990) USSR Chironomidae, Amphipoda, Fish eggs Bogatova ( I USSR Chironomidae Boikova (1 986) USSR Chaoborus, Cyclopoida, Leptodora, Trichoptera Boron & Kuklinska (1 987) Germany Chironomidae, Cladocera, Copepoda Brabrand (1 Norway Chironomidae, Cladocera & Vetkasov ( 1974) USSR Chironomidae, Crustacea, Fish eggs Hansson ( 1984) Sweden Chironomidae, Amphipoda, Mollusca Hansson ( 1987) Sweden Cammarus, Pontoporeia, Insecta larvae Holker & Hammer ( 1994) Germany Neomysis, Crangon crangon, Eurvtemora Jamet ( 1994) France Macroinvertebrates Johnsen ( 1965) Denmark Chironomidae, Crustacea, Amphipoda Kangur & Kangur ( 1996) Estonia Chironomidae, Cladocera, Copepoda Kolomin ( 1977) USSR Chironomidae, Trichoptera, Mollusca Kozlova & Panasenko (1 978) USSR Chironomidae, Insecta larvae, Crustacea Meisriemler ( I Sweden Chironomidae, Gammarus Nagy (1986) Germany Chironomidae, Ephemeroptera, Crustacea Nagy ( 1988) Germany Chironomidae Ogle et a/. ( 1995) USA Chironomidae, Ephemeroptera, Crustacea Nilsson (1979) Sweden Pontoporeiu, Mvsis, Chironomidae Palle ( Denmark Chironomidae Pliszka & Dziekonska ( Poland Chironomidae Polivannaya (1 974) Russia Copepoda. Cladocera, Chironomidae Schiemenz ( Germany Chironomidae Continued Biology and Life History of Ruffe 177

TABLE 3. Continued. Author Country Major Food Items Shamardina ( USSR Chironomidae, Chaoborus, Cyclopoida Smirnova ( USSR Chironomidae, Chaoborus, Cyclopoida Van Densen ( 1985) Netherlands Chironomidae, Amphipoda, Crustacea Willemsen (1 977) Netherlands Chironomidae, Gammarus Winfield et al. (1996) U.K. Bosmina, Chironomidae Winfield et al. (1 996) U.K. Asellus, Chironomidae

alternative prey, Asellus aquaticus, which ruffe con- 1986). On a species level, some species of chirono- sumed mostly. Several major diet studies found egg mids may be selected against (Nagy 1986). In addi- predation by ruffe to be low or nonexistent tion, age-0 ruffe may select larger Daphnia and (Johnsen 1965; Hansson 1984; Nagy 1986, 1988; copepods (Van Densen 1985). In contrast, Johansson Boron and Kuklinska 1987; Ogle et al. 1995), even and Persson (1986) concluded that ruffe consume though eggs can be identified in the stomach for 1 organisms, and Kangur and Kangur (1 996) found to 3 days after being eaten (Sterligova and that ruffe consumed Chironomus plumosus, in pro- Pavlovskiy 1984). Ruffe have been implicated in portion to their abundance in the benthos. the decline of Coregonus stocks on several occa- Adult ruffe probably feed in the shallow littoral sions (Pokrovskii 1961, Balagurova 1963, Adams zone (Leszczynski 1963, Holcik and Mihalik 1968, and Tippett 1991), but good evidence beyond a cor- Boron and Kuklinska 1987, Jamet and Lair 1991). relation has not been provided. Holcik and Mihalik (1968) and Ogle et al. (1995) The diet of ruffe differs little due to lake trophic concluded that ruffe move from deeper to shallower status, within-lake location, or ruffe density. Ruffe waters at night to feed. Bagge and Hakkari (1985) fed mainly on chironomids and ephemeropterans in suggested that ruffe feed in deeper waters during lakes of moderate and high productivity, although the summer than during other times of the year. diet breadth was greater in the more productive Ruffe appear capable of feeding at all times of day lakes (Bergman 199 1). Bergman and Greenberg (Bergman 1988, Ogle et al. 1995), but on some (1994) determined that ruffe diet consisted of days may only feed at dusk, night, or dawn (Westin mostly macrobenthos at all levels of ruffe density, and Aneer 1987, Jamet and Lair 1991, Ogle et al. with only the contribution of trichopterans and Pi- 1995). Adams and Tippett (1991) did not observe sidium affected by ruffe density. Differences in diel feeding periodicity by ruffe during winter. ruffe diet between sampling locations were ob- The sensitive cephalic lateral line and visual sys- served in some situations (Hansson 1987, Nilsson tems may both be used by ruffe to detect and locate 1979), but not others (Hansson 1984, Ogle 1992). prey. Kuiper (1967) found that ruffe could localize In general ruffe change their diet little after immobile prey that were made mobile by “involun- switching to feeding primarily on macrobenthos tary trembling of the hand” and that electromag- early in life (Collette et al. 1977, Rosch et al. netic stimulation of nerves attached to the cupulae 1996). This is supported by observations by caused ruffe to “snap for food.” Physiological stud- Bergman (1988) for three size classes of ruffe, ies indicate that the ruffe lateral line could detect Boron and Kuklinska (1987) for age-1 and older and locate chironomid larvae in the top layers of the ruffe, and Jamet and Lair (1991) for age-2 and older bottom substrate at a distance 2 to 5 cm from it’s ruffe. However, Boikova (1986) identified a slight snout (Denton and Gray 1989, Gray and Best shift in diet composition at a length of 8 to 10 cm 1989). The organization of the cone cells in the reti- and Ogle et al. (1995) identified a similar shift at a nae and presence of the tapetum lucidum are con- length of 12 cm. sistent with the bottom-feeding behavior of ruffe in Little information is available regarding prey se- low-light conditions (Ahlbert 1970). Furthermore, lection by ruffe. Juvenile and adult ruffe may select ruffe have relatively high levels of choleacetyltrans- chironomids, ephemeropterans, and Sialis spp. ferase and acetycholine levels in the brain, which (Leszczynski 1963, Nagy 1986, Bergman 1990, are typical of fish with well-developed visual sys- Bergman and Greenberg 1994), but select against tems (Szabo et al. 199 1 ). However, the square cone oligochaets and Hirudinea (Leszczynski 1963, Nagy pattern is indicative of poor movement perception 178 Derek H. Ogle

(Ahlbert 1970) and the reaction distance of ruffe is ing ability; thus, ruffe should have a competitive only 4 cm, compared to 21 cm for Eurasian perch advantage (Bergman and Greenberg 1994). (Bergman 1987). Bergman and Greenberg (1994) concluded that Elshoud-Odenhave and Osse (1976) described ruffe and Eurasian perch compete for food re- two types of feeding and thoroughly describe the sources because an increasing density of ruffe and a physiology and behavior related to these two types. constant density of roach (in enclosures) caused Backlifting-type feeding occurs when the ruffe Eurasian perch to eat more zooplankton, thus slow- senses the prey on the bottom, approaches the prey, ing their growth. Evidence for intraspecific compe- lifts and curves the body while above the prey, and tition has also been shown (Hansson 1985, sucks the prey into its mouth. Horizontal-type feed- Bergman and Greenberg 1994). ing occurs when the ruffe senses the prey floating A prerequisite for competition is the ability of a in the water-column, approaches it from below, and fish to reduce prey biomass. Mattila and Bonsdorff sucks it into its mouth. (1 989) suggested, based on feeding rates deter- The effect of temperature and light on capture mined in the laboratory, that ruffe should be able to rate, handling time, and swimming performance structure the benthic community through predation. were examined by Bergman (1987, 1988). Handling However, in a weakly designed experiment, they time decreased, capture rate increased, and swim- found no effect of ruffe on the abundance or com- ming performance remained constant with increas- position of the bottom fauna. Bergman (1990) and ing temperature (Bergman 1987). Maximum Bergman and Greenberg (1994) found that Sialis capture rate and swimming speed decreased with spp., a preferred food item of ruffe, were reduced decreasing light levels (Bergman 1988). When significantly in enclosures containing ruffe. Nagiec compared to Eurasian perch, ruffe were affected (1977) suggested that a depauperate benthos may less by temperature and light and had a much have been caused by ruffe, bream, or eel (Anguilla shorter reaction distance (4 cm compared to 20 cm; anguilla). Bergman 1987, 1988). PREDATORS COMPETITORS In Europe and Asia, ruffe are eaten by only a few Ruffe likely compete for food resources with predators. The primary predators of ruffe are other benthivorous fish, including bream (Abramis pikeperch (Stizostedion lucioperca; Deedler and brama; Boikova 1986), white bream (Blicca bjo- Willemsen 1964, Holcik and Mihalik 1968, Biro erkna; Zadorozhnaya 1978), Coregonus spp. (Hans- 1971, Fedorova and Vetkasov 1974, Bonar 1977, son 1984, Winfield 1992), roach (Rutilus rutilus; Marshall 1977, Popova and Sytina 1977) and north- Duncan 1990), sturgeon (Acipenser rutherns; ern pike (Esox lucius; Vollestad 1986, Eklov and Sokolov and Vasil'ev 1989), smelt, trout-perch Hamrin 1989, Adams 199 1, Pervozvanskiy and (Percopsis omiscomaycus; Ogle et al. 1995, Sier- Bugayev 1992, Ogle et al. 1996). Fish that eat ruffe szen et al. 1996), Eurasian perch (Thorpe 1977, in small quantities are eel, burbot (Lota lota), white Bergman and Greenberg 1994), and yellow perch bream, lake trout (Salvelinus namaycush), small- (Ogle et al. 1995). Only interactions between ruffe, mouth bass (Micropterus dolomieu), black crappie roach, and Eurasian perch have been studied exten- (Pomoxis nigromaculatus), bullheads (Ictalurus sively. Diet overlap between ruffe and roach is low spp.), walleye (Stizostedion vitreum), Eurasian (Hansson 1984), roach growth was unaffected by perch, and yellow perch (Johnsen 1965; Popova and ruffe density (Bergman and Greenberg 1994), and Sytina 1977; Rundberg 1977; Willemsen 1977; Ko- ruffe growth and diet composition was not affected zlova and Panasenko 1977; Zadorozhnaya 1978; by roach (Bergman 1990). However, Duncan Nilsson 1979, 1985; de Nie 1987; Ogle et al. 1996). ( 1990) found that the abundance of ruffe increased Rare instances of cannibalization have been docu- after Eurasian perch and roach abundance declined mented (Johnsen 1965). In addition, ruffe are eaten due to a viral infection. Diet overlap between ruffe by cormorants (Phalacrocorax carbo; Van Dobben and Eurasian perch was substantial in a Baltic arch- 1952), kingfishers (Alcedo atthis; Hallet 1977), and ipelago (Hansson 1984) and in Lake Aydat, France smew (Mergus albellus; Doornbos 1979). (Jamet 1994). Ruffe foraging ability is not as af- The rate of' predation on ruffe is affected by the fected by light (Bergman 1988) and temperature abundance of ruffe and the availability of alterna- (Bergman 1987) as much as Eurasian perch forag- tive prey. Pikeperch generally consume more ruffe Biology and Life History of Ruffe 179 in years when the abundance of smelt, their pre- Pokrovskii 196 I) and Corylurus (Swennen et al. ferred prey, is low (Popova and Sytina 1977, 1979) have been reported. Dactylogyrus amphi- Willemsen 1977). For example, Pihu and Pihu bothrium were apparently transferred to the U.S. (1974; as cited in Popova and Sytina 1977) found with ruffe (Cone et al. 1994). that ruffe were 10 to 15% of the annual ration of Abnormalities of the liver (Kranz and Peters pikeperch in years when smelt were abundant and 1984, Peters et al. 1987), fins (Lindesjoo and 80 to 85% in years when smelt were scarce. Thulin 1990, Thulin et al. 1988, Weissenberg Eurasian perch also consume more ruffe when 1965), and jaws and opercula (Weissenberg 1965) smelt are scarce (Popova and Sytina 1977). In Loch have been documented. Many of the ruffe with ab- Lomond, the diet of northern pike shifted from normalities were collected in polluted waters (i.e., Coregonus lavaretus to ruffe after ruffe were intro- kraft mill effluent, PCB contamination). duced and their population expanded (Adams 199 1). Walleye, conditioned to eat soft-rayed fish POSSIBLE POPULATION CONTROL or offered soft-rayed fish as an alternative, con- sumed few ruffe (Ogle et al. 1996). It is difficult to reduce the numbers of ruffe be- Ruffe have a wide array of adaptations to avoid cause they have several adaptations to compensate predation. The most conspicuous of these adapta- for high mortality rates (Lind 1977) and would tions are the large dorsal, anal, pelvic, and preoper- likely quickly rebound (Lelek 1987). For example, cular spines. Spines make a small forage fish ruffe may grow quickly, mature early, and spawn appear larger than it actually is, especially to a more than once in a season. Thus, few efforts to predator that attacks the center of a prey mass control ruffe have been carried out and those that (Webb and Skadsen 1980, Eklov and Hamrin 1989). have, have met varied success. Spines also require the predator to swallow the fish Some intentional or unintentional changes in pis- head first, thus limiting the attack to the head and civorous abundance have sometimes resulted in de- may puncture the throat or stomach lining (Eklov creased levels of ruffe. Stocking of elvers and and Hamrin 1989, Lammens et al. 1990). In addi- protective regulations for pikeperch and eel resulted tion, ruffe are equipped with a retinal tapetum lu- in a 5- to 7-fold decline in ruffe catches in Lake cidum that allows ruffe to see predators in low-light Vortsjarv, Estonia (Pihu 1982, Pihu and Maemets twilight conditions (Ahlbert 1970) and numerous 1982). A decrease in potential ruffe predators due lateral-line sensors that are sensitive to large wave- to overfishing led to a sudden rise in the abundance length disturbances from predators (Collette et al. of “small coarse fish,” including ruffe, in some 1977). Finally, cryptic coloration and living near Russian waters (Popova and Sytina 1977). Ruffe the bottom may reduce predation. also became abundant in London reservoirs follow- ing the loss of predatory fish to viral infections (Duncan 1990); however, a cause-and-effect rela- PARASITES AND PATHOLOGY tionship is not evident in this case because benthiv- Ogle (1992) compiled a list of 63 parasites of orous roach also declined. The catch of ruffe from the published literature and “undesirable fish,” which includes ruffe, was posi- Bykhovskaya-Pavlovskaya et al. (1 964) provided a tively correlated to the yield of predatory fish (eel, comprehensive list of ruffe parasites in Russia. pikeperch, and pike) in some Polish waters (Bonar Only those parasites that were common or had 1977); however, it is impossible to determine if known impacts will be discussed here. The cesto- ruffe actually declined. In contrast, the termination dian (a liver parasite) Triaenophorus nodulosus of the gillnet fishery in Lake Tjeukemeer, the (Bagge and Hakkari 1982), the nematode Anguilli- Netherlands resulted in significantly more and cola crassus (Hoglund and Thomas 1992, Thomas larger pikeperch, but catches of ruffe were not af- and Ollevier 1992), the monogonean (a gill para- fected (Lammens et ul. 1990). Predation on ruffe site) Dactylogyrus amphibothrium (Izyumova 1958, did not increase in Lake Tjeukemeer, because the Valtonen et ul. 1990) and the fluke Cotylurus varie- abundance of smelt, the preferred prey of gatus (Swennen et al. 1979) were common on ruffe pikeperch, was not linked to pikeperch numbers be- in some instances. In most situations, no pathologi- cause smelt immigrate from an adjoining lake. In cal effects were observed (e.g., Haenen and Van the St. Louis River, United Slates, walleye and Banning 1990). However, massive dieoffs due to northern pike were stocked aggressively and their infections by the flukes Tetracotyle (Johnsen 1965, harvest was curtailed in hopes that the two pisci- 180 Derek H. Ogle vores would keep ruffe numbers low. However, tion pressure following the introduction of ruffe, walleye and northern pike consumed few ruffe dur- Gymnocephalus cernuus (L.) to Loch Lomond. J. Fish ing the initial invasion period (Ogle et al. 1996). In Biol. 38:663-667. Lake Vortsjarv, intensive removal of ruffe by bot- and Tippett., R. 1991. Powan, Coregonus lavare- tom trawling did not decrease ruffe numbers (Pihu tus (L.), ova predation by newly introduced ruffe, 1982, Pihu and Maemets 1982). Gymnocephalus cernuus (L.), in Loch Lomond, Scot- In some instances, the abundance of ruffe may be land. Aquac. Fish. Man. 22:239-246. Ahlbert, I.B. 1970. The organization of the cone cells in limited by benthos production. Ruffe were present the retinae of four teleosts with different feeding in low numbers in Lake Vastra Kyrksundet, Fin- habits (Perca fluviatilis L., Lucioperca lucioperca L., land, it was meromictic (Bonsdorff and Stor- when Acerina cernua L. and Coregonus albula L.). Arkiv berg 1990); however, ruffe biomass increased when Zoologi 22:445-48 I. the lake became limnic and benthos production Aleksandrova, A.I. 1974. A morphological and ecologi- increased. cal description of ruffe [Acerina cernua (L.)] of the middle reaches of the Dneiper. J. Ichthyol. 14:53-59. CONCLUSIONS Ali, M.A., Ryder, R.A., and Anctil, M. 1977. Photore- ceptors and visual pigments as related to behavioural Ruffe appear to be remarkably adaptable to a responses and preferred habitats of perches (Perca wide variety of conditions as evidenced by the large spp.) and pikeperches (Stizostedion spp.). J. Fish. Res. amount of variability in many of the biological and Board Can. 34: 1475-1480. life history traits examined here. Morphological American Fisheries Society. 199 1. Common and scien- characteristics varied across large geographical tific names of fishes from the United States and scales, within certain water bodies, and between Canada. American Fisheries Society Special Publica- sexes. Ruffe tolerated a wide variety of conditions tion 20. Bethesda, Maryland. including fresh and brackish waters, lacustrine and Anttila, R. 1973. Effects of sewage on the fish fauna in lotic systems, depths of 0.25 to 85 m, montane and the Helsinki area. Oikos (suppl) 15:226-229. submontane areas, and oligotrophic to eutrophic Appelberg, M. 1990. Population regulation of the cray- waters. Age and size at maturity differed according fish Astacus astacus L. after liming an oligotrophic, to temperature and levels of mortality. Ruffe low-alkaline forest lake. Limnologica 20:3 19-327. spawned on a variety of substrates, for extended pe- Bagge, P., and L. Hakkari. 1982. The food and parasites riods of time, and in some instances, may have of fish in some deep basins of northern Lake Paijanne. spawned more than once per year. Growth of ruffe Hydrobiologia 86:6 1-65. and Hakkari, L. 1985. Fish fauna of stony shores varies by sex, morphotype, water type, intraspecific of Lake Saimaa (Southeastern Finland) before and density, and food supply. Interactions with other during the floods (1980-82). Aqua Fennica 15: species (i.e., competition and predation) appeared 237-244. to vary considerably between systems. Bakanov, A.I., Kiyashko, V.I., M.M., and Strel’nikov, A.S. 1987. Factors affecting fish growth. ACKNOWLEDGMENTS J. Ichthyol. 27: 124-1 32. Balagurova, M.V. 1963. 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