Hydrobiologia 312 : 27-35, 1995 .© 1995 Kluwer Academic Publishers . Printed in Belgium .

An isolated population of fourhorn sculpins (Myoxocephalus quadricornis,family Cottidae) in a hypersaline high arctic Canadian lake

Mike DickmanEcology and Biodiversity Department, Hong Kong University, Pokfulam Road, Hong Kong

Received 23 March 1994 ; in revised form 20 September 1994 ; accepted 4 October 1994

Key words : mining impacts, sculpins, cephalic spines, evolution

Abstract

Freshwater sculpins probably evolved from marine ancestors which entered bodies of water such as proglaciallakes or lakes which were gradually isolated from the sea by isostatic rebound . Sculpins in fresh water lakes(Myoxocephalus thompsoni [Girard]) lack cephalic horns and live well below a depth of 10 m . Those in the sea(Myoxocephalus quadricornis [Linnaeus]) typically live above 10 m and possess a well developed set of fourcephalic horns . The sculpins in Garrow Lake, North West Territories, are intermediate between the marine andfresh water forms with respect to their depth distributions and their cephalic horns (spines) . As a consequence,Garrow Lake, which separated from the sea some 3000 years ago, serves as an excellent `laboratory' for studyingevolutionary changes in this sculpin . The age of the lake was based on carbon-14 dates of the fossil pelecypodsfrom raised beaches around the lake and from observations of rates of isostatic rebound in the area as reported byDickman & Ouellet 1983 and Page et al. 1984. During the last 3000 years, the surface waters of Garrow Lake havefreshened and its sculpins have apparently adapted to this top down freshening by occupying a depth where thesalinity of the lake approaches that of sea water. As a result, the sculpin population in Garrow Lake lives deeperthan the sculpin population in the nearby Garrow Bay . Thus, the deeper dwelling Garrow Lake sculpins appear tobe less vulnerable to avian predation than their shallow water dwelling marine ancestors . It is hypothesized thatreduced avian predation of the Garrow Lake sculpin population is associated with the observed reduction in theircephalic horns which impart a certain degree of disruptive colouration and disruptive pattern outline allowing theshallow dwelling marine species to blend in with its background in a manner which appears to make it less visibleto avian predators .

It is unfortunate that the three thousand year old Garrow Lake sculpin population is now endangered by minetailings entering the lake from the nearby Cominco Ltd . mine. The entire food chain of the lake appears to havebeen severely impacted by lead and zinc mine tailings entering Garrow Lake at a rate of 100 metric tonnes per hour .

Introduction

According to McAllister, the continental lacus-trine deepwater sculpin (Myoxocephalus thompsoniand the marine forms of this genus, the fourhornsculpin (Myoxocephalus quadricornis), are distinctspecies whose ranges do not overlap (McAllister &Aniskowitz, 1976) . The `marine' fourhorn sculpinsometimes enters estuaries or rivers but does not per-manently reside in lakes . McAllister & Aniskowicz(1976) presented evidence from vertebral counts whichappears to refute the hypothesis that Arctic coast and

27

island sculpin populations were derived from mainlanddeep water sculpin populations . Champagne, Haring-ton & McAllister (1979) reported a 10000 year-oldfossil of the deep water sculpin that was found nearOttawa, Canada. McAllister (1961), referred to thefreshwater species as the `deep water sculpin' . TheMyoxocephalus thompsoni fossil was just as taxonom-ically distinct from Myoxocephalus quadricornis asare the present day freshwater populations . This sug-gests that Myoxocephalus thompsoni is perhaps pre-Wisconsin in age .

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LITTLE CORNWALLIS ISLAND

OV

POLARIS

McDOUGALLSOUND

I

..l

Tem ple ton..

Bay

Fig . 1 A . Little Cornwallis Island, N .W.T., at 75 ° 23' N ; 96 ° 50' W. with inset of Hudson Bay, Greenland and Davis Strait (modified fromEnergy Mines and Resources NTS map No . 6814-8) .

The fourhorn sculpin (Myoxocephalusquadricornis)

M. quadricornis is a circumpolar marine species rang-ing from the Barent Sea to the Bering Sea in thePalearctic and from Labrador and James Bay toEllesmere Island in the nearctic . M. quadricornis ispresent in Greenland but absent in Iceland, Norway,and Spitzbergen (McAllister, 197 8) . As an adult, it mayattain a maximum size of 34 cm in total length, but themean size is usually considerably smaller (ibid) .

M. quadricornis is found in salt and brackishcoastal waters at depths of 0-20 m and is also found inestuaries and up rivers as far as 150 km from the sea(McAllister, 1978) . M. quadricornis apparently doesnot form resident populations in fresh water (ibid) .Eggs hatch in May and June (Khan & Faber, 1973) .Adults feed on crustaceans, annelids (primarily tubifi-cids), pelecypods, chironomids, and fish . M. quadri-cornis are preyed on by mergansers, loons, herons,grebes, gulls, Lota Iota (ling cod), Myoxocephalusscorpius (shorthorn sculpin), Salvelinus alpinus (Arc-

tic char), and the northern pike, Esox lucioides, (McAI-lister & Aniskowicz, 1976) .

The deepwater sculpin (Myoxocephalusthompsoni)

M. thompsoni were probably derived from M. quadri-cornis at the beginning of the Wisconsin glaciationor earlier. Its taxonomy and distribution have beendescribed by McAllister (1961) and McAllister &Aniskowicz (1976) . Discriminant function analysis by(McAllister, 1978) permitted the separation of all spec-imens of the two species M. thompsoni and M. quadri-cornis that were previously treated by Bailey (1970) asconspecific .

Fig. I B. Morphometric map of Garrow Lake, modified from a COMINCO Ltd . (1979) map. Isobaths are in metres .

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M. thompsoni occupies deep and cool water main-land lakes within or near basins of former glacial lakes,from the Great Lakes and the Ottawa River drainageswest and north to Great Bear Lake, Northwest Territo-ries (Scott & Crossman, 1973) . The deepwater sculpin,live landlocked in deep, cold water lakes in northernNorth America . McPhail & Lindsey (1970) have sum-marized a good deal of information about their biology.M. thompsoni distributions in lakes Superior, Michi-gan, and Huron are not accurately represented becauseextensive areas have not yet been surveyed . It prob-ably inhabits all parts where water depth is suitable(McAllister, 1961) . M. thompsoni adults and juvenilesare primarily benthic and according to Johnson (1975)they occupy the entire floor of the Great Bear Lake

Fig. I C. B.C. Research seining for sculpins in Garrow Lake, August, 1981.

Fig. 2 A. A typical fourhorn sculpin from Garrow Bay.

Fig. 2 A-1 . Profile of the head of the marine sculpin, M. quadricor-nis, with its conspicuous cephalic horns .

from depths of 3 m to the deepest parts of the lake . Inthe

Great Lakes, M. thompsoni generally avoids shal-low water, occurring mainly at depths of 50 m and isusually found at low temperatures in well oxygenat-ed waters (McAllister, 1978) . Adults feed mostly onPontoporeia and Mysis . Myoxocephalus thompsoni arepreyed upon by Salvelinus namaycush and Lota Iota(ibid). Khan claims that deepwater sculpin larvae dis-perse widely into open water shortly after hatching .Thus planktonic juveniles and bottom dwelling adults,occupy different habitats and different niches (Khan,1971) .

Description of the study lake

Garrow Lake (Fig. IA, lB and 1C) has an area of418 ha, maximum depth of 47 m, and is ice coveredto a maximum thickness of 2 .4 m for more than 11months of the year (Fallis & Harbicht, 1980 ; Dick-man & Ouellet, 1983) . The profundal-zone salinity ofthis ultraoligotrophic, meromictic lake is 75 parts perthousand (Dickman & Ouellet, 1987) . As a result ofthis high salinity, the water in the bottom of the lakenever turns over. This accounts for the presence of apermanent anaerobic zone occurring below a depth of20 m in Garrow Lake. The top of this anaerobic zoneis occupied by a dense layer of phototrophic bacteria(Dickman et al . 1990) .

Methods

During the period 1980-1987, the Polar ContinentalShelf Project and the Natural Sciences and Engineer-ing Research Council supported numerous studies of

J&Z'

I

3 1

Fig. 2 B. Deepwater sculpin from Lake Michigan . Drawing basedon specimens from the National Museum of Canada and informationfrom Scott and Crossman (1973) .

Garrow Lake. Working with a team of other scientists, Iwas able to sample the lake during August 1980, 1981,1982, June 1984 and August 1987 . Water chemistry,phytoplankton and zooplankton samples were taken oneach of these trips, fish and benthos were sampled in1981 and 1987 (Dickman & Ouellet, 1987) .

Fish were captured in 5-15 m of water using agraded series of gill nets from 2 .54-10 .16 cm (I to 4inches) mesh size with lead lines which kept the baseof the gill net on the bottom of the lake . Nets were setat depths of 3, 5, 7, 12, 15 and 18 m . Specimens werepreserved in 10% formalin solution and examined atBrock University .

Photographs and drawings of the fourhorn sculpin(Figs 2A and 2A-1) were based in part on specimentsprovided by the Royal Ontario Museum in Toronto,Canada. Photographs and drawings of the deepwatersculpin (Fig. 2B) were based on specimens provided bythe National Museum of Natural Sciences in Ottawa.Shrinkage of formalin preserved specimens was nottaken into account in the presentation of meristic data,and, as a result, all meristic measures were roundedto the nearest whole number. Photographs and draw-ings of the Garrow Lake sculpin (Fig . 2C and 2C-1)were based on specimens removed from Garrow Lakebetween 1980 and 1987 . All water samples were tak-en using a 2 litre Van Dorn water sampler and thewater was transferred to new half litre Nalgene plas-tic bottles which had been twice rinsed with the waterwith which they were to be filled . Dissolved oxygen,pH, temperature and specific conductivity and salinitywere measured in the field using a Y.S.I . conductivitymeter (model 51 A) and a Y S .I . dissolved oxygen meter(model 33) and/or a Hydrolab 4000 oxygen, tempera-ture, pH, specific conductivity .

Plankton samples were taken from the mixolimnionas well as from the top of the monimolimnion (20 m) .Samples were filtered through either a 0.45 micronNucleopore, Millipore or Whatman GF/C filters . Inthe laboratory, the Whatman glass GF/C filters were

Fig. 2 C. A typical fourhom sculpin from Garrow Lake.

Fig. 2 C-I. Profile of the head of the Garrow Lake sculpin, M. quadricomis, with its reduced cephalic horns.

homogenized by sonification for 15 minutes in a solu- tion of acetone, methanol and water (80%, 15% and 5% volume/volume respectively) using a model W-375 Ultrasonic sonicator. The supernatant was analyzed for bacteriochlorophyll pigments and bacteriochloro- phyll decomposition products using an A minco DW- 2-UVNTS scanning spectrophotometer.

Results

Fourhorn sculpins in Garrow Lake range in depth from 5 to 15 m. These depths correspond with a salinity range of 0.1 to 1.1 times the salinity of sea water (Dick- man & Ouellet, 1987). Due to the sculpins' preference

for low temperature, and high dissolved oxygen (Scott & Crossman, 1973), the Garrow Lake fourhorn sculpin is restricted to a narrow depth range corresponding to its temperature, salinity, oxygen and dissolved oxygen preference ranges. Below 15 m the temperature rapid- ly increases reaching 8.9 ' C at 20 m and dissolved oxygen rapidly declines to zero at 20 m (Dickman & Ouellet, 1987).

Nets set below 15 m or above 5 m had no M. quadri- cornis in them and those set at 15 m had only one or two individuals in them. In Garrow Lake, the majority of the sculpins were caught in nets set at 7 to 12 m. A total of 23 adults were caught and measured. The largest adult measured 17 cm, the smallest was 9.1 cm (values rounded to the nearest third significant figure) and the mean length was 11.2 cm (Table 1).

Discussion

The length of the cephalic spines of the Garrow Lake population (n = 23) are intermediate. (spine length = 0.13 cm, Table 1). Deepwater sculpins have no cephalic spines and those of the marine fourhorn sculpin (0.23 cm from base to tip) represent the longest spines. In addition, the body length of these three groups of sculpins also differ quite signifi- cantly. The deepwater sculpin is the smallest (body length=6.8 cm). The Garrow Lake individuals were

0

0

0

0

0

17

again intermediate (body length= 11 .3 cm) and themean length of the 27 marine fourhorn sculpins thatwere measured was 12 .6 cm (Table 1) .

Although the deepwater sculpin has no cephalicspines, the Great Lakes and other cold water lakeswhere it lives are not predator free . Dymond (1926)recorded as many as 27 deepwater sculpins from a sin-gle lake trout stomach, the average number per stomachbeing 5 .4 . As many as 32 were recorded from a single

33

burbot stomach, the average number per stomach being11.2 (Scott & Crossman, 1973) . Thus the presence ofcephalic spines can not be attributed to piscivore pre-dation intensity . Alternatively, if the cephalic spinesserve primarily to reduce avian predation losses bymaking the shallow dwelling marine individuals lessconspicuous to an avian predator (disruptive patternoutline), their absence in deepwater sculpins wouldresult from the fact that M. thompsoni lives at depths

Table 1 .

Length of the Garrow Lake sculpins (cm)

Mean :

Std. Dev . :

Std. Error: Variance : Coef. Var. : Count:11 .248

2.409

0.502 5.802 21 .415 23Minimum: Maximum : Range : Sum : Sum of Sqr. :9 .1

17

7.9 258 .7 3037 .45

Length of the marine sculpins (cm)

Mean: Std . Dev . : Std . Error: Variance : Coef . Var. : Count:

12.575 4.442 0.855 18 .564 35 .321 27Minimum: Maximum : Range : Sum : Sum of Sqr. :9 .66 22.5 12 .84 339 .535 4782.735

Length of the freshwater sculpins (cm)

Mean: Std . Dev . : Std. Error: Variance : Coef. Var. : Count :

6.794 2.298 0.557 5 .279 23 .46 17Minimum: Maximum : Range : Sum : Sum of Sqr. :

5 .9 7 .5 1 .6 66 .5 715 .19

Garrow Lake sculpin spine height (cm)

Mean : Std. Dev . : Std. Error: Variance : Coef. Var. : Count :.129 .114 0 .022 0.013 94 .12 23Minimum: Maximum : Range : Sum : Sum of Sqr. :.03 0 .41 0 .38

Marine sculpin spine height (cm)

Mean : Std. Dev. : Std . Error: Variance : Coef. Var. : Count :.226 .219 .029 0.048 96.72 27Minimum : Maximum : Range : Sum : Sum of Sqr. :.05 0 .91 0 .86 13 .362 5.809

Freshwater sculpin spine height (cm)Mean : Std . Dev. : Std . Error : Variance: Coef. Var . : Count :

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greater than those normally frequented by avian preda-tors. In the Great Lakes, M. thompsoni (referred to asM. quadricornis by Scott & Crossman, 1973) general-ly avoids shallow water, occurring mainly at depths of50 m or more and is usually found at low temperaturesin waters less than 5 °C (McAllister, 1978) . M. quadri-cornis, by contrast, live in shallow waters and avianpredation by gulls, loons, herons, grebes, mergansersetc. can be quite significant (ibid) .

Atrophy of cephalic spines in the freshwater form ofthe fourhorn sculpinComparative anatomy is replete with examples ofstructures which are small or useless but which previ-ously were large and served important functions . Somesnakes, for example, have claw-like appendages ontheir bodies which prove to be the remains of vesti-gial lizard-like hind legs that have almost disappeared(Colinvaux, 1986) . Man's vestigial appendix is all thatis left of an intestinal organ which reached its greatestsize in plant-eating animals such as kangaroos and rab-bits (ibid) . The old adage of : `use it or loose it' is basicto this notion of vestigial parts . It is tempting to con-clude that the same process is at work on the `horns'of the sculpins in Garrow Lake . This assumes that theprimitive form is the long horned marine species . Inthe absence of an avian predator, the large cephalicspines of the fourhorn sculpin would appear to impartdisruptive patterns on the outline of the Garrow Lakesculpins but this would be of little value in light of theirgreater depth distribution in Garrow Lake . Accordingto this scenario, an individual which produced a smallor spindly set of cephalic spines (Fig . 2A) would notbe at a particular selective disadvantage . If the energysaved by not forming large spines was funneled insteadinto increased egg production, for example, then selec-tion for the reduced spine morph would occur .

The perfection of cryptic appearances and attitudesto avoid detection by predators will always remain animpressive testament to the force and pervasiveness ofnatural selection (Ricklefs, 1973) . One means for anorganism to attain crypsis is by matching the colour andbackground pattern and texture of the substrate uponwhich it rests . Another means of attaining crypsis isfor the organism to be marked with disruptive patternsand textures to obliterate the telltale outlines of its bodyagainst the background (Colinvaux, 1986) . The uniquecontribution of this paper is that it attempts to estimatethe length of time that a cryptic pattern which is nolonger of selective value has taken to change .

In fresh water, the deep water sculpin, as its nameimplies, lives below the depths frequented by mostavian predators. In the ocean, the fourhorn sculpin livesin very shallow waters where its cephalic spines arepresumed to afford it added disruptive body patternsmaking it less discernible to avian predators .

By spending most of their time below a depth of 5 mthe fourhorn sculpin in Garrow Lake escapes detec-tion by most avian predators . This is not the casefor populations from the nearby Garrow Bay whichwere observed at 1 m or less . Cormorants, herons andloons preying on the shallow water dwelling fourhornsculpins have been observed by numerous researchers(Harbicht, Pers. Comm.). Thus, if the club shapedspines on top of the head ofM. quadricornis (Fig. 2A-1) serve to reduce avian predation losses, these spineswould be of less significance in Garrow Lake due tothe greater depths that this sculpin occupies . If, as aresult of this habitat preference change, the spines havelittle survival value, their reduction (Figs 2B and 2C)would be plausible. However, few studies are availableto document the rate of spine reduction . It was suggest-ed (Mandrak, 1990) that deep water sculpins living inHeney Lake as well as other proglacial lakes have losttheir cephalic spines over the last 12 000 years . Thusthe partial loss of cephalic spines in Garrow Lake overthe last 3000 years, while rapid in terms of geologicaltime for evolution, is credible in terms of the proglaciallake atrophy of all cephalic spines over the last 12 000years .

Conclusions

The salinity, temperature, and dissolved-oxygen pro-files for Garrow Lake (Dickman & Ouellet, 1987)reflect four depth-zones : (1) a 0-5 m deep mixolimnionwith low salinity (<I ppt) associated with fresh waterrunoff and ice melt-water. This zone is saturated withdissolved oxygen ; (2) a 5-12 m brackish-water zonewith saturated and supersaturated dissolved oxygenand increasing salinity . The majority of the M. quadri-cornis in Garrow Lake are associated with this zone ;(3) a 12-20 m deep chemocline (chemolimnion) dis-playing a strong salinity gradient and rapidly decreas-ing dissolved oxygen ; and (4) an anaerobic zone (20-47 m) with hypersaline water (2 .3 times the salinity ofsea water). Oxygen in the bottom layer (20-47 m) wasconsistently zero over the period 1980 to 1987 . Theanaerobic zone was capped by a mass of phototrophicbacteria (Dickman & Ouellet, 1983, 1987) which con-stitute the major primary producer in the lake .

It would appear that the observed increase in sur-face water concentrations of lead and zinc (Dickman,1991) coupled with a dramatic reduction in the abun-dance of the population of the major primary producerin Garrow Lake, will likely lead to the extirpation ofthe lake's fourhorn sculpin population . This is unfor-tunate because the natural selection in the fourhornsculpins in Garrow Lake makes the lake a fascinating`laboratory' for the study of natural selection .

Acknowledgments

I am grateful to E. J. Crossman, N . E. Mandrak andR. Winterbottom of the Royal Ontario Museum andD. McAllister of the National Museum of Canada forthe loan of freshwater and marine fourhorn sculpins .I am also grateful to each of the above and to H . Fer-nando of the University of Waterloo, Ontario Canadafor their constructive comments on preliminary draftsof this manuscript. Museum specimens were measuredby F. Fiore and E. Mortier who received EnvironmentalYouth Corps funding . I am also grateful to NSERC andthe Department of Indian Affairs and Northern Devel-opment's Polar Continental Shelf Project for logisti-cal and financial support for this project . S. Harbictand B. Fallis of Environment Canada provided helpfuladvice about the sculpin population in Garrow Lakewhich they and B . C. Research had collected .

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