Functional Convergence Among Pelagic Sculpins of Lake Baikal and Deepwater Ciscoes of the Great Lakes

J. Great Lakes Res. 25(4):847–855 Internat. Assoc. Great Lakes Res., 1999

Functional Convergence Among Pelagic Sculpins of Lake Baikal and Deepwater Ciscoes of the Great Lakes Randy L. Eshenroder1,*, Valentina G. Sideleva2, and Thomas N. Todd3 1Great

Lakes Fishery Commission 2100 Commonwealth Blvd., Suite 209 Ann Arbor, Michigan 48105 2Zoological

Institute Russian Academy of Sciences St. Petersburg 199034, Russia 3Great

Lakes Science Center—USGS/BRD 1451 Green Road Ann Arbor, Michigan 48105

ABSTRACT. The vast, well-oxygenated hypolimnia of Lake Baikal and the Great Lakes were both dominated by endemic planktivorous fishes. These dominants, two species of sculpins (Comephorus, Comephoridae) in Lake Baikal and six species of deepwater ciscoes (Coregonus, Salmonidae) in the Great Lakes, although distant taxonomically, have morphologies suggesting a surprising degree of functional convergence. Here it is proposed that the same two buoyancy-regulation strategies observed in Baikal sculpins also arose in the deepwater ciscoes of the Great Lakes. One strategy favors hydrostatic lift (generated by low specific gravity) and is characterized by fatter, larger-bodied fish with smaller paired fins; the second strategy favors hydrodynamic lift (generated by swimming) and is characterized by leaner, smaller-bodied fish with larger paired fins. Both types likely evolved to feed on a single species of ecologically analogous, vertically migrating macrozooplankter: Macrohectopus branickii in Lake Baikal and Mysis relicta in the Great Lakes. It is suggested that Coregonus did not diversify and proliferate in Lake Baikal as they did in the Great Lakes because by the time Coregonus colonized Lake Baikal, pelagic sculpins were already dominant. INDEX WORDS: Baikal, Great Lakes, Cottoidei, Coregonus, evolution, glacial refugia, species flock, diel vertical migration, buoyancy regulation, emergent property.

INTRODUCTION Lake Baikal is the largest lake by volume and the oldest lake in the world. All of the Laurentian Great Lakes are among the top-twenty lakes in size, but they are considerably younger (Beeton 1984). The southern basin of Lake Baikal, the oldest and deepest part of the lake, formed in a rift 30 Mya during the Oligocene (Mats 1993) whereas the Great Lakes basin was deglaciated only at the end of the Pleistocene (~0.01 Mya). Both systems have exceptionally deep and well-oxygenated hypolimnia. Lake Baikal has a maximum depth of 1,741 m and Lake

*Corresponding

Superior, the deepest of the Great Lakes, has a maximum depth of 407 m. Hypolimnia of this size are a rare environment for freshwater fishes capable of migrating freely within the water column. Typically, the fish that flourish in such waters are closely related species that evolved within the system (endemics) from ancestral taxa that were often strikingly different among lakes (Sideleva 1994). In Lake Baikal this environment, the deepwater pelagia, is dominated by sculpins, a lineage of fishes (Cottoidei, Perciformes) typically associated with a sedentary, bottom existence in both marine and fresh waters. In contrast, the deep waters of the Great Lakes were historically dominated by ciscoes (Coregonus,

author. E-mail: [email protected]

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Salmonidae), common planktivores in recently glaciated Holarctic lakes. Why different taxa, sculpins and ciscoes, radiated in the deepwater pelagia of these two systems is puzzling. Lake Baikal is inhabited by one species of cisco, the omul (Coregonus autumnalis migratorius), and also by the European whitefish (C. laveretus) (Kozhov 1963), a species noted for diversification, and the Great Lakes are inhabited by four species of sculpins. If sculpins and ciscoes were in each lake at the same time, the same taxon would presumably have radiated in both lakes, but, in fact, opposite taxa radiated in each system. The vast marine-like hypolimnia of Lake Baikal and the Great Lakes should favor selection of similar traits in deepwater planktivores. Gradual gradients of temperature, light, and pressure and a near absence of structure are physical features of these cold, dark waters. Across these limited gradients, zooplankters may be dispersed and may also vertically migrate thereby favoring planktivore capability for nightly ascents akin in range to those made by marine mesopelagic fishes. The objectives of this paper are to describe important traits of the pelagic sculpins of Lake Baikal and of the deepwater ciscoes of the Great Lakes that appear to result from functional convergence and to identify the associated selection pressures. The paper will focus mainly on traits associated with diel vertical migration. Some of the inferences are speculative especially for types of deepwater ciscoes that were extirpated before they were well studied. The functional biology of the pelagic sculpins in Lake Baikal is well-documented in the literature whereas deepwater ciscoes, even extant species, have received less attention. OVERVIEW OF ECOLOGY Lake Baikal This paper focuses on the two species of fully pelagic Baikal sculpins, the big oilfish (Comephorus baicalensis) and the little oilfish (C. dybowskii ) (Fig. 1). They are members of a diverse species flock comprising 36 species and subspecies (Taliev 1955, Smith and Todd 1984). All sculpins except the oilfishes and two semi-pelagic species (Cottocomephorus spp.) are benthic forms that inhabit the lake bottom to various depths to 1,600 m (Taliev 1955, Brauer et al. 1984). All Baikal sculpins except the oilfishes are oviparous and spawn on the lake bottom. The oilfishes are ovoviviparous

FIG. 1. The Lake Baikal oilfishes: Comephorous baicalensis (top) and C. dybowskii (bottom).

(termed viviparous in Russian literature); the embryos, resulting from internal fertilization, develop in the ovary and the eggs hatch when they emerge from the genital opening as free-swimming larvae. The big oilfish is the largest fish in the deepwater pelagia; females reach a length of 220 mm, males 145 mm. Little oilfish achieve lengths of 160 mm (Chernyayev 1974). The oilfishes can be considered the most ecologically important fish in Lake Baikal. They occupy more of the volume of the lake than any other species; the depth ranges of the two oilfishes broadly overlap extending from 1,500 m to 250 m for the big oilfish and to 150 m for the little oilfish (Taliev 1955, Sideleva et al. 1993). Both species make diel vertical migrations at night that involve ascents of up to 500 m (Chernyayev 1974). Smirnova (1995) states that the biomass of oilfishes comprises 70% of the total ichthyofauna of the lake. The food chain in the deepwater pelagia of Lake Baikal is characteristically simple for ancient lakes (Dumont 1994). A copepod, Epischura biacalensis, and a planktivorous amphipod, Macrohectopus branickii, both endemics, are by far the main zooplankters. Macrohectopus ascends to the surface at night to feed on Epischura (Rudstam et al. 1992). The amount of each zooplankter in the oilfish diet depends on predator-to-prey size ratios. In turn, the oil fishes are prey for the Baikal seal (Phoca sibirica), the only large piscivore. The oilfishes also feed on small fishes including their own young.

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FIG. 2. The deepwater ciscoes of the Great Lakes sized as from Lake Michigan (from Koelz 1929). Great Lakes Six species (incipient species) of deepwater ciscoes (Fig. 2) historically dominated the deepwater pelagia in the Great Lakes, but three of these are considered extinct, and the three extant species occur together now only in Lake Superior (Todd and Smith 1992). Todd and Smith (1992) considered five of the six species to be endemics, but the exception, the more-widespread Coregonus zenithicus, lacks unique mtDNA (Sajdak and Phillips 1997) and rDNA (Reed et al. 1998) sequences anticipated in a species that survived the last glaciation, although subsequent hybridization may have obscured evidence of divergence (Smith 1992). How many of the deepwater ciscoes predate the Wisconsinan is unresolved. The lake herring or shallow water cisco (C. artedi) is the presumed ancestor of at least three of the species (Todd and Smith 1992) and possibly all six if C. zenithicus is endemic; it has both shallow and deepwater populations in Lake Superior. Therefore, in the Great Lakes, unlike in Lake Baikal, the ancestral species (the lake herring) and its descendents have widely overlapping depth distributions. Depletions of deepwater ciscoes early in this cen-

tury, especially of the deepest-dwelling species, precludes estimation of their historical contribution to the fish biomass in any Great Lake. In Lake Michgan, the bloater (C. hoyi), the sole surviving deepwater cisco, comprised about 75% of plantivore biomass in 1987 (Argyle 1992), but this species does not occupy the deepest water formerly inhabited by the extinct species (reviewed in Eshenroder and Burnham-Curtis 1999). This and other observations, especially those in Koelz’s (1929) monograph, indicate that historically the deepwater ciscoes, like the pelagic sculpins in Lake Baikal, were ecological dominants. Adult ciscoes were considerably larger in size than the pelagic Baikal sculpins. Koelz (1929) reported a maximun length of 386 mm for the largest species (the blackfin, C. nigripinnis) and 285 mm for the smallest species (the bloater) in Lake Michigan, but the largest ciscoes were already fished out by the time of his study. The reproductive biology of the deepwater ciscoes is less-well understood than that of the Baikal sculpins. All of the deepwater ciscoes spawned on the bottom generally in deep water (Koelz 1926). Inasmuch as the fry and juveniles of the bloater oc-

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cupy surface waters (Crowder and Crawford 1984), the other ciscoes in this closely related group may have similar life histories (Crowder 1980). The deepwater cisco food chain is more complex than that of the Baikal sculpins. Only limited diet data exist for any of the deepwater ciscoes except for the bloater. Bloater juveniles feed on a variety of cladocerans and copepods and adults consume increasing numbers (with depth) of amphipods (Diporeia spp.) and Mysis relicta (reviewed in Wells and Beeton 1963, Crowder and Crawford 1984). Mysis, like Macrohectopus, is a planktivore that ascends toward the surface at night. Bloaters in Lake Michigan also make nightly ascents (TeWinkel and Fleischer 1998), and Eshenroder et al. (1998) inferred that this behavior is a feature of deepwater cisco evolution. The deepwater ciscoes were eaten by burbot (Lota lota) and lake trout (Salvelinus namaycush) (Van Oosten and Deason 1938). Piscivory on the deepwater ciscoes and the oilfishes differs spatially in that burbot and lake trout inhabit the entire cisco depth range whereas the Baikal seal typically dives to depths of only 10 to 50 m but occasionally descends to 300 m (Stewart et al. 1996). IMPORTANCE OF BUOYANCY REGULATION In this section background is provided on buoyancy adaptations (Gee 1983, Alexander 1993, and Pelster 1997) because of their importance as evolved traits in the oilfishes and deepwater ciscoes. Fish that live in the water column must expend energy to keep from sinking if their density exceeds the density of their environment. Adaptations to minimize the resulting energetic costs are generally of two types. The first type of adaptation generates hydrostatic lift by incorporation of lessdense tissues and/or by reduction of heavy tissues especially bone. The second type generates hydrodynamic lift from the force of swimming. The swim bladder, a hallmark trait of teleost evolution, provides the greatest possible compensation for heavy tissues, but it presents limitations for fish that make extensive vertical migrations. Swim bladder volume changes in response to pressure so that as a fish ascends its bladder expands and with descent contracts. Diel vertically migrating (DVM) fish typically maintain enough gas in their swim bladder so that they are near neutral buoyancy at the top of an ascent (usually made at night) and are not neutrally buoyant on descent. The loss of buoyancy when descended diminishes the value of the

swim bladder for fish that DVM. Also, a fish risks being carried helpless to the surface if it ascends too far in the water column and its swim bladder over inflates. Physostomous fish like ciscoes that retain the pneumatic duct have only weak gas-secreting and absorbing capability. Fahlen (1959) described a primitive-type of rete mirabile in the European whitefish (C. lavaretus), but even fish with well-developed retes (physoclists) cannot produce enough gas to maintain neutral buoyancy when undertaking extensive DVM. Therefore, extensive DVM favors selection for traits in addition to the swim bladder to create lift. Of particular interest in the oilfishes and ciscoes are accumulations of lipids (the specific gravity of fish triglycerides is generally around 0.92), loss of bone mass (specific gravity of freshwater-fish bone ranges from 1.57 to 2.04), and modified fins that slow the rate of sinking. CONVERGED TRAITS Hydrostatic Lift Selection for density reduction was especially important in the evolution of the Baikal oilfishes as their immediate ancestors like other Cottoidei were negatively buoyant. Cottoidei are heavy fish without swim bladders, having been selected to resist displacement from substrates by moving water. Several tissues have been modified in the oilfishes to reduce density. Big oilfish bone is 55% less mineralized (based on ashed skeleton weights) than bone in benthic Cottoidei, and lipid levels (wet weight) in adults are as high as 44.3% (Sideleva 1994, 1996), although Ju et al. (1997) reported a maximum lipid content of 34.5%. With a specific gravity of 1.040, the little oilfish is less buoyant; lipid levels in adults range from 4 to 12% (Sideleva et al. 1993). The maximum lipid level found by Ju et al. (1997) for the little oilfish, 2.1%, is again below that reported in the Russian literature. The little oilfish is classified as a buoyantly heavy fish whereas adult big oilfishes are classified as light (specific gravity very near 1.000). The deepwater ciscoes of the Great Lakes were noted for their fattiness and it was this distinguishing trait that made extensive fisheries based on smoked-fish products possible. Unfortunately, these fisheries were so extensive that the largest-bodied ciscoes, which were preferred for their higher fat levels, were seriously over-fished before the turn of the century (Koelz 1926), thus preempting much research on them. Lipid levels are known only for a

Functional Convergence of Sculpins and Ciscoes single species of deepwater cisco, the bloater, a small-bodied species. Rowan and Rasmussen (1992) found that mean lipid levels for commercial-sized bloaters from all three upper Great Lakes varied between 12.1 and 22.0%. The maximum lipid content reported for the bloater is 24.8% (Hesselberg et al.1990). In contrast, lake herring (a possible ancestor of the bloater) from the Great Lakes were found by Rowan and Rasmussen (1992) to have mean lipid levels that varied from only 6.1 to 12.6%. As is typical for Salmonidae, the largest bloaters are also the fattest so that the larger-bodied, extinct species of deepwater ciscoes likely had lipid accumulations even greater than those reported for the bloater. Bone mass of bloaters and lake herring has not been studied, so any selection in the bloater for reduced mineralization is unknown. Selection for reduced density in the bloater, at least as evidenced by increased lipids, was apparently accompanied by a reduction in swim bladder size. ANCOVA was used to compare swim bladder length against standard length (standard length ranged from 80 to 160 mm) for juvenile bloaters and lake herring reared in captivity under the same conditions. A model with an interaction term between species and standard length showed that slopes were not significantly different (p = 0.596) indicating that swim bladder length increased at the same rate for both species. Without the interaction term, the model showed that bloater swim bladders were significantly shorter than lake herring bladders by 3.3 mm on average (n = 24, p = 0.002, r 2 = 0.826) (Fig. 3). If the bloater evolved from the lake herring, then the swim bladder of the bloater should be proportionately smaller (shorter) than the bladder in lake herring to offset the extra lift provided by higher levels of lipids in bloaters. Selection for increased lipids without a corresponding reduction in swim bladder size would result in positive buoyancy, which is as energetically costly as negative buoyancy for planktivores and not favored by selection. Hydrodynamic Lift The most striking external feature of the oilfishes is the size of their fins (Fig. 1), which are much larger than in benthic Cottoidei. The massive pectoral fins in both oilfishes are associated with a form of swimming called beat-and-glide, which Weihs (1973) theorized can provide energy savings of over 50%. As viewed from submersibles, oilfish thrust is developed by undulations of the posterior

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FIG. 3. Swim bladder length versus standard length (mm) for bloaters and lake herring spawned from Lake Michigan parents and reared in captivity (ANCOVA, r2 = 0.826, p = 0.002). half of the body with the pectoral fins nearly retracted but at an angle to the direction of movement. Water passing over the angled fins creates lift. With dissipation of forward motion (the end of the beat phase), the pectoral fins are fully extended and the gliding phase begins (Sideleva et al. 1993). When extended, the large pectorals slow sinking, which conserves energy otherwise expended for lift. The enlarged second dorsal and anal fins are passive during the beat phase (Sideleva et al. 1993), and apparently provide a larger vertical surface for generating thrust from trunk undulations. Oilfishes assume a stationary head-down position (perpendicular or oblique to the water surface) when observed during the day apparently to facilitate detection of prey while presenting a reduced silhouette to predators striking from below (Pankhurst et al. 1994). Differences in fin sizes between the big and little oilfishes coincide with the differences in body density and behavior of these species. The pectoral fins of the little oilfish are 2.5 times as large as those of the big oilfish in relation to the body surface area of each species. Likewise, the second dorsal and anal fins of the little oilfish together are 1.5 times as large as those of the big oilfish in relation to body surface area (Sideleva et al. 1993). Having bigger fins, the little oilfish is better adapted for beat-and-

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glide swimming than the big oilfish. Little oilfish are heavy and must constantly swim to generate lift whereas adult big oilfish are light and can maintain position in the water column without swimming. These differences in anatomy and behavior show that the two oilfishes evolved distinct buoyancy strategies to function as planktivores in Lake Baikal. Similar buoyancy strategies appear to have also evolved among the deepwater ciscoes. The kiyi (Coregonus kiyi), a small-bodied cisco that typically inhabits deeper water, is comparatively thin and was not esteemed by the commercial smokers (Koelz 1929). This description suggests that the kiyi differs from the other deepwater ciscoes in lipid accumulations in the same way that the little oilfish, which is buoyantly heavy, differs from the buoyantly light big oilfish. Among the deepwater ciscoes, the kiyi clearly has the longest paired fins, but the differences in fin sizes among deepwater ciscoes are not as remarkable as they are for oilfishes. Koelz’s (1929) measurements show that kiyi pectorals were approximately 12 to 32% longer (depending on species) than pectorals of the other deepwater ciscoes and pelvics were 15 to 27% longer. The swimming behavior of the kiyi has not been observed under conditions that favor beat-andglide swimming, i. e., when fish are descended and swim bladders are compressed. If the kiyi undertakes DVM as does the bloater (Eshenroder et al. 1998), its closest relative (Todd and Smith 1992), deepwater ciscoes display the same buoyancy-regulation strategies as the oilfishes: a fat, larger-bodied form with smaller fins and a lean smaller-bodied form with larger fins. Behavior Diel vertical migration itself may be a converged trait of oilfishes and deepwater ciscoes. Both taxa appear to have evolved to prey on diel vertically migrating macrozooplankters: Macrohectopus in Lake Baikal and Mysis in the Great Lakes. Eshenroder and Burnham-Curtis (in press) argued that speciation of the deepwater ciscoes was a response to the great abundance of Mysis in the deeper waters of the Great Lakes and to their extensive vertical migration. Sideleva (1994) advanced a similar hypothesis connecting the evolution of the oilfishes with the availability of Macrohectopus. Both macrozooplankters undertake extensive vertical migration (Beeton 1960, Rudstam et al. 1992). The ability of a planktivore to migrate with its prey is

considered advantageous (Janssen and Brandt 1980). DISCUSSION This paper has advanced the idea that the same two buoyancy strategies recognized in the Baikal oilfishes evolved also in the deepwater ciscoes of the Great Lakes. One strategy involves reliance primarily on obtaining lift from lipid accumulations and the other relies primarily on lift from beat-andglide swimming. Evidence for two buoyancy strategies in the oilfishes is based on both morphology and behavior whereas in the deepwater ciscoes the behavior (DVM) associated with the morphologies has been observed in only a single species (the bloater). It is assumed that all of the deepwater ciscoes were selected for DVM and that the elongated paired fins of the kiyi are an adaptation for beatand-glide swimming. Evidence for functional convergence between the oilfishes and the deepwater ciscoes is mostly indirect. In fact, without knowledge of oilfish biology the evolution of similar buoyancy-regulation strategies in deepwater ciscoes would not have been inferred. Evolution of similar traits associated with DVM in oilfishes and deepwater ciscoes, however, is not surprising. The vast hypolimnia of both systems are dominated by macrozooplankters that are functional and morphological analogues (Rudstam et al. 1992, 1998). Functional convergence of planktivores in the two systems may occur because of common selection pressures—abundant macrozooplankters with space for extensive vertical migration. The more challenging questions emerging from these comparisons are why such markedly different taxa radiated in each system and what are the larger implications of planktivore convergence. Why sculpins radiated in Lake Baikal instead of ciscoes is intriguing. This paradox of secondarily pelagic forms radiating to dominance was also raised by Clarke and Johnston (1996) for Antarctic nototheneids (Perciformes). The modifications required to convert a shallow-water cisco into a deepwater cisco are trivial compared to the evolved differences between benthic sculpins and oilfishes. Oilfishes exhibit laterally compressed bodies (probably to improve swimming performance (Webb 1992)), loss of pigments, a reshaped mouth for feeding on larger prey (Sideleva 1994), changes in retinas and in the position of the eyes (Bowmaker et al. 1994, Pankhurst et al. 1994), pelagic spawning, and internal fertilization and egg incubation

Functional Convergence of Sculpins and Ciscoes (Chernyayev 1974). In contrast, ancestors to the deepwater ciscoes were already advanced pelagics whose swim bladders provided hydrostatic lift. The simplest explanation for the dominance of oilfishes in Lake Baikal is that the omul and European whitefish gained entry to Lake Baikal after the oilfishes were already highly specialized. If the Baikal omul and whitefish had the same potential for differentiation as did Great Lakes ciscoes, they should have proliferated quickly (as did Great Lakes ciscoes) and hindered oilfish speciation. The omul is genetically differentiated from the widespread Arctic cisco (C. a. autumnalis) more than the Arctic cisco differs from the lake herring (Bodaly et al. 1994), indicating residence in Lake Baikal since at least the late Pleistocene. But, Sukhanova et al. (1996) using mtDNA and Mamontov and Yakhnenko (1998) using allozymes detected only minor genetic differentiation among the three recognized forms of omul in Lake Baikal, which suggests more recent entry. Differentiation, however, may be retarded in river-spawning/ dwelling fish like the omul as compared to lake fishes, a phenomenon hinted at by Smith and Todd (1984) and more fully developed in an oral paper given in 1995 by Bodaly (Freshwater Institute, 501 Crescent Street, Winnipeg, Manitoba R3T 2N6). Therefore, low genetic distance and the modest phenotypic separation among omuls (Bronte et al. 1999) may reflect constraints on intrapopulation differentiation in river-spawning fish. Whitefish have apparently inhabited Lake Baikal since at least 0.6 to 0.7 Mya (Slobodyanyuk et al. 1994), but genetic distance between the two extant forms, lake and lake-river, is minor (Mamontov and Yakhnenko 1995, 1998). These authors show that the lake form is more genetically diverse than the lake-river form. They also attribute the low level of genetic differentiation to population bottlenecks during the (late) Pleistocene and to hybridization with omuls. Although Lake Baikal itself was not glaciated, it would have cooled considerably (it contained icebergs), and its northern tributaries would have been blocked by glaciers (see Mats 1993). Glaciation likewise may have bottlenecked omul differentiation. It cannot conclusively be shown that oilfishes originated before omuls and whitefish entered Lake Baikal. Slobodyanyuk et al.(1995) indicate that the oilfishes evolved 1.2 to 1.8 Mya, and Hunt et al. (1997) report a somewhat older age (2.4 Mya). Both studies provide much older times of residence than indicated by intrapopulation genetic distance

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between the two coregonids. Although coregonids were likely in Lake Baikal much longer than the genetic studies indicate, their differentiation in Lake Baikal was apparently setback by glaciation, which may have affected the oilfishes less. Once the oilfishes were well established, they could have inhibited coregonid colonization of deep water. Oilfish adaptations for buoyancy regulation are more advanced than those of the omul and whitefish, and here it was assumed that they were already more advanced when Coregonus colonized Lake Baikal. In fact, the big oilfish is one of only two species of freshwater fish reported to be neutrally buoyant without a functional swim bladder, the other species being the siscowet lake trout of Lake Superior (Crawford 1966). The question of coregonid and sculpin residency in the Great Lakes is less problematical than in Lake Baikal. Both taxa entered shortly after the end of the Pleistocene. Sculpins would at best have had only hundreds of years to radiate before deepwater ciscoes evolved. In North America, a larger controversy exists as to the age of endemic planktivores in part because of the problem of identifying suitable refugia lakes (Bailey and Smith 1981). Where would such highly specialized forms like the deepwater ciscoes persist during glacials, and if they did persist in shallower waters, would specializations for vertical migration be lost and then reevolve during interglacials? Radiations of endemic planktivores like the oilfishes and deepwater ciscoes can be viewed as markers for freshwater pelagia with exceptional depths and volumes. The selection pressures in such systems favor specialized traits that result in speciation and in a dominance of endemic fish. Such radiations can be viewed as emergent properties of these systems. Endemicity may be the rule for large, deep lakes because sources for pre-adapted colonists would be from similar systems that are so rare that migratory connections are unlikely. The endemic planktivores of Lake Baikal and the Great Lakes can be considered to be among the most important elements of the fish biodiversity in these lakes. They provide a structure in the pelagia that otherwise would not exist. Now that the deepest-dwelling ciscoes are extinct in Lake Michigan (Todd and Smith 1992), its deep pelagia is essentially uninhabited by planktivores during the season of fish growth (Brandt et al. 1991, Argyle 1992). This zone, which encompasses waters beyond a depth of approximately 80 m and extends from just off of the bottom to the metalimnion, comprises

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over half the volume of the lake. A loss of the oilfishes from Lake Baikal would result in an even larger depopulation. Pelagic food webs in large systems like Lake Baikal and the Great Lakes are particularly vulnerable to disruption because they depend on only a few species so specialized that they are unlikely to be replaced by other indigenous fishes. The conservation of such species is clearly a priority. ACKNOWLEDGMENTS Camille Ward and Ann Krause helped with the regression analysis. Lars Rudstam and Gerry Smith provided peer reviews. This article is Contribution 1085 of the USGS Great Lakes Science Center. REFERENCES Alexander, R.M. 1993. Buoyancy. In The Physiology of Fishes, ed. D.H. Evans, pp.75–97. Ann Arbor, MI: CRC Press. Argyle, R.L. 1992. Acoustics as a tool for the assessment of Great Lakes forage fishes. Fish. Res. 14:179–196. Bailey, R.M., and Smith, G.R. 1981. Origin and geography of the fish fauna of the Laurentian Great Lakes basin. Can. J. Fish. Aquat. Sci. 12:1539–1561. Beeton, A.M. 1960. The vertical migration of Mysis relicta in Lakes Huron and Michigan. J. Fish. Res. Board Can. 17(4):517–539. ———. 1984. The world’s great lakes. J. Great Lakes Res. 10(2):106–113. Bodaly, R.A., Vuorinen, D.A., Reshetnikov, Yu. S., and Reist, J.D. 1994. Genetic relationships of five species of coregonid fishes from Siberia. J. Ichthyol. 34(6):117–129. Bowmaker, J.U., Govardovskii, V.J., Shukolyukov, S.A., Zueva, L.V., Hunt, D.M., Sideleva, V.G., and Smirnova, O.G. 1994. Visual pigments and the photic environment of the cottoid fish of Lake Baikal. Vision Res. 34(5):591–605. Brandt, S.B., Mason, D.M., Patrick, E.V., Argyle, R.L., Wells, L., Unger, P.A., and Stewart, D.J. 1991. Acoustic measures of the abundance and size of pelagic planktivores in Lake Michigan. Can. J. Fish. Aquat. Sci. 48(5):894–908. Brauer, R.W., Sideleva, V.G., Dail, M.B., Galazii, G.I., and Roer, R.D. 1984. Physiological adaptation of cottoid fishes of Lake Baikal to abyssal depths. Comp. Biochem. Physiol. 77A(4):699–705. Bronte, C.R., Fleischer, G.W., Maistrenko, S.G., and Pronin, N.M. 1999. Stock structure of Lake Baikal omul as determined by whole-body morphology. J. Fish Biol. 54:787–798. Chernyayev, Zh.A. 1974. Morphological and ecological features of the reproduction and development of the

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