Journal of Fish Biology (2002) 60, 000–000 doi:10.1006/jfbi.2002.2179, available online at http://www.idealibrary.com on
Morphological variation between lake- and stream-dwelling rock bass and pumpkinseed populations
J. B* M. G. F†‡ *Ontario Ministry of Natural Resources, Sudbury, Ontario, P3G 1E7, Canada and †Environmental & Resource Studies Program and Department of Biology, Trent University, Peterborough, Ontario, K9J 7B8, Canada
(Received 11 March 2002, Accepted 22 October 2002)
Pumpkinseed Lepomis gibbosus and rock bass Ambloplites rupestris stream populations of both sexes were significantly different in external morphology from lake populations in a central Ontario, Canada, watershed. The predictions that stream fishes would be more slender-bodied, and have a more anterior placement of lateral fins than lake fishes were generally supported. The prediction that stream fishes would have a more robust caudal peduncle was partially supported. The prediction that fin size would be larger in stream fishes was not supported, as lake rock bass generally had longer and wider fins than those from stream sites. The results suggest that in some species, smaller fins may be favoured in stream-dwelling individuals because the reduction of drag during swimming more than compensates for their reduced power and propulsion efficiency in a current. Smaller fin size in stream-dwelling centrarchids may be related to their body shape, or to their low usage of fast-moving water within the streams they inhabit. 2002 Published by Elsevier Science Ltd on behalf of The Fisheries Society of the British Isles.
Key words: adaptation; body shape; centrarchids; fin size; running water.
INTRODUCTION Variation in the ecological strategies used by different populations of the same fish species, and by different species, are commonly observed at a variety of geographical scales. Evidence for these divergent strategies has been demon- strated across large geographical scales, including differences observed across a continent (Gross, 1979), and among watersheds (Bodaly, 1979; Baltz & Moyle, 1981; Hindar & Jonsson, 1982). Different ecological strategies can also be observed at much smaller scales, such as those observed between populations from different habitat types within a single lake (Hindar & Jonsson, 1982; Robinson et al., 1993), or stream (Beacham et al., 1989; McLaughlin & Grant, 1994; McLaughlin & Noakes, 1998). Divergent morphological strategies have been documented in a number of fish species, including pumpkinseed Lepomis gibbosus (L.) (Robinson et al., 1993), bluegill Lepomis macrochirus Rafinesque (Ehlinger & Wilson, 1988), various sticklebacks (Gross, 1979; Lavin & McPhail, 1993), Arctic charr Salvelinus alpinus (L.) (Hindar & Jonsson, 1982), brook charr, Salvelinus fontinalis (Mitchill) (McLaughlin & Grant, 1994), and Trinidadian guppies Poecilia reticulata (Peters) (Robinson & Wilson, 1995). ‡Author to whom correspondence should be addressed. Tel.: +1 705 748 1011; fax +1 705 748 1569; email: [email protected] 1 0022–1112/02/000000+00 $35.00/0 2002 Published by Elsevier Science Ltd on behalf of The Fisheries Society of the British Isles. 2 . . .
While morphological divergence in many of these species has been docu- mented in either lake or stream environments, few studies have compared the morphology of lake and stream dwelling populations within a species. Stream environments offer greater variation in habitat type and structure, a less predictable frequency of catastrophic events (Baltz & Moyle, 1982; Ryder & Pesendorfer, 1989), and more arduous hydrodynamic conditions (Baltz & Moyle, 1982; McLaughlin & Grant, 1994) as compared to lakes. Gross (1979) compared the morphology of ninespine sticklebacks Pungitius pungitius (L.) from 16 stream, lake and marine sites across Europe, but the comparisons were primarily based on meristic counts rather than morphometric measurements. Similarly, a study of tule perch Hysterocarpus traski Gibbons morphology (Baltz & Moyle, 1981) was based primarily on meristic traits (only four morphometric measures were used), and significant differences were found among three geographically isolated watersheds, rather than between stream and lake sites per se. Lavin & McPhail (1993) compared the morphology of threespine sticklebacks Gasterosteus aculeatus L. inhabiting streams and lakes in British Columbia using meristic traits and morphometric measures. Although the stream fish were observed to be smaller and deeper-bodied, many of the morphological differences were related to the feeding ecology of the fish, rather than to water flow. One comparative study that was more focused on mor- phology (rather than meristic traits) was of juvenile coho salmon Oncorhynchus kisutch (Walbaum) reared in stream and lake habitats (Swain & Holtby, 1989). This study related the observed morphological differences to factors other than water flow; in this case, schooling in the lakes and territoriality in the streams. In the present study, the morphology of lake and stream populations of two centrarchid species were compared and related to the presence or absence of flowing water. It was hypothesized that stream populations will have morpho- logical characteristics that produce less drag on the fish and allow for stronger swimming in the current of lotic ecosystems. Four predictions developed from hydrodynamic theory or from studies of stream populations (mainly of salmonids) were tested: (1) stream fishes will be more slender-bodied than their lake counterparts to reduce drag when swimming into the current (Webb, 1984; McLaughlin & Grant, 1994; McLaughlin & Noakes, 1998); (2) stream fishes will have longer and wider pelvic, pectoral, anal and dorsal fins to improve their manoeuvrability and stability in a current (Beacham et al., 1989; Swain & Holtby, 1989); (3) the caudal peduncle of stream fishes will be more robust (Webb, 1984), with a lesser depth (McLaughlin & Grant, 1994), but a greater width to accommodate a greater muscle mass; (4) the lateral fins of stream fishes will be more anterior in position than those of lake fishes to improve their ability to orientate in current, and to assist with strong, steady swimming (Webb, 1984; Swain & Holtby, 1989). The species used in this study were the pumpkinseed and the rock bass Ambloplites rupestris (Rafinesque). The pumpkinseed is native to east-central North America. While it is often the most abundant species in small lakes, ponds and slow, quiet streams in Ontario (Scott & Crossman, 1973), it can also be found in streams with a moderate velocity (0·3–0·5 m s1; pers. obs.). The rock bass is also a common species, and is also found in stream and lake environments throughout east-central North America (Scott & Crossman, 1973). 3
Pumpkinseed and rock bass are gibbose in body form, in contrast to the fusiform salmonids, upon which most studies of morphological adaptation to flowing water are based. The gibbose form is more highly adapted to complex manoeuvring in lentic environments than to swimming in a current (Webb, 1998). The examination of morphological traits of gibbose fishes in flowing water provides a broader understanding of the adaptation of fishes to hydro- dynamic forces. Furthermore, unlike many of the salmonid species used in morphological studies, neither the pumpkinseed nor the rock bass are territorial, except for nesting males. Therefore, morphological differences between lake and stream populations of pumpkinseed and rock bass are more likely to be due to the presence or absence of flow than to social differences that occur in these different habitats.
MATERIALS AND METHODS STUDY DESIGN AND STUDY SITES Differences in fish morphology between streams and lakes were assessed with a paired stream–lake design, with fishes sampled from a given stream compared to those from an adjacent lake in the same watershed. By comparing fishes in proximal waterbodies within the same watershed, the potential effect of geographic distance (Gross, 1979), climate (Lotspeich, 1980) and watershed differences (Baltz & Moyle, 1981, 1982) on aspects of the ecology and life history of the fishes were minimized. The stream–lake pairs used in this study were Indian River (4414 N; 789 W)–Rice Lake (4412 N; 788 W) and Eels Creek (4436 N; 785 W)–Stony Lake (4435 N; 783 W) (Fig. 1). These waterbodies are part of the Kawartha Lakes region of central Ontario, Canada, located c. 110 km north-east of Toronto. The Kawartha Lakes are part of the Trent–Severn Waterway, which connects Georgian Bay (Lake Huron) to the Bay of Quinte in Lake Ontario. Rice Lake is a shallow lake with a surface area of c. 100 km2, an average depth of 2·4 m and a maximum depth of 10·0 m. The lake can be considered eutrophic, with a mean summer chlorophyll a concentration of 14·6 gl1 and a mean Secchi disk depth of 1·9 m (1995–96 data from Mercer et al., 1999). Most parts of the lake are covered by thick macrophyte beds that consist largely of Eurasian watermilfoil Myriophyllum spicatum, curley leaved pondweed Potamogeton crispus, waterweed Elodea canadensis, tapegrass Vallisneria americana and coontail Ceratophyllum demersum (Wile, 1974). Some nearshore areas of the lake are largely devoid of vegetation due to wave action and the clearing of beaches. The Indian River flows south into Rice Lake, entering the lake near the village of Keene. Like many of the rivers entering the Trent–Severn system, flow is controlled by a number of dams along the length of the river. The predominant land use in the watershed is agriculture, and runoff from the land makes this a relatively productive river. Stony Lake has a surface area of c. 28·2 km2 and a mean depth of 5·9 m. The lake is divided into two basins: a shallow, more productive west basin, and a deeper, less productive east basin. Stony Lake is less nutrient-enriched than Rice Lake, perhaps because the mixed deciduous–coniferous forests of the north shore are largely intact, agriculture is less predominant in the watershed, and the portion of the watershed north of the lake is located on the relatively nutrient poor soils of the Canadian Shield (Wile & Hitchin, 1976). A mean total phosphorus concentration of 10 gl1 was recorded for Stony Lake in the summer of 1976, while the mean chlorophyll a concentration was 3·9 gl1 and the Secchi disk depth was 4·3 m (Wile & Hitchin, 1976). More recent limnological data for Stony Lake are unavailable, but the lake would probably be considered as mesotrophic at the time of study. The aquatic vegetation of Stony Lake is more sparse than in Rice Lake, and the predominant species of submerged vegetation are 4 . . .
Eels Creek N
Stony Lake
Drummer Lake Clear Lake
Lakefield
Indian River
Ouse R.
Peterborough Hastings
Keene Otonabee R.
Rice Lake
0 5 10 km
F. 1. Location of waterbodies used in this study. Symbols refer to sites where pumpkinseed only (), rock bass only () or both species ( ) were sampled.
pondweeds (Potamogeton spp.), Eurasian watermilfoil, coontail, muskgrass (Chara spp.), waterweed (Elodea spp.), tapegrass and pickerelweed Pontederia cordata (Wile, 1974). Eels Creek flows in a southerly direction into the east basin of Stony Lake. The watershed is located on the granite of the Canadian Shield, and the surrounding vegetation is predominantly composed of coniferous and mixed forests. The flow of Eels Creek is largely unregulated in comparison to other rivers in the Kawarthas, which, combined with the impermeable underlying rocks, causes periodic severe spring flood events. Such an event occurred in the spring of 1998 prior to field sampling (K. Irwin, pers. comm.). The productivity of Eels Creek is substantially lower than that of Indian River because of the differences in watershed characteristics. The soils of the Eels Creek watershed are thin and relatively infertile, and the extensive forests are largely intact. 5
T I. Fish collection dates and sample sizes
Size range Species Site Dates collected Sample Size LS (mm)
Pumpkinseed Indian River 11–27 August 1997 23 14 50·9–102·6 5–12 June 1998 3 1 72·5–102·0 Rice Lake—unvegetated 25–26 May 1998 34 50 58·1–138·2 Rice Lake—vegetated 26–28 May 1998 31 49 61·8–137·7 Rock Bass Indian River 5–12 June 1998 39 40 62·8–189·0 Rice Lake 28 May–4 June 1998 44 42 70·8–155·6 Eels Creek 15–18 June 1998 43 46 64·5–139·4 Stony Lake 18–26 June 1998 42 27 63·8–152·8
FISH COLLECTION AND HABITAT ASSESSMENT All fishes were sampled in the late spring and early summer of 1998, except for the Indian River pumpkinseed population, most of which were collected in August 1997 (Table I). In the spring of 1998, pumpkinseeds were collected from vegetated and unvegetated sites on Rice Lake to compare morphological differences between these habitat types. While these samples could be used to make the morphological comparison with Indian River, a sufficient number of pumpkinseeds from Eels Creek could not be collected to make the second stream–lake comparison. For this reason, no pumpkinseeds were collected from Stony Lake, and the stream–lake comparison for this species was restricted to a single set of paired waterbodies. The location of all sample sites is indicated on Fig. 1. Sites were selected using four criteria: abundance of pumpkinseed and rock bass, suitable water velocity, site accessibility and the presence of similar physical habitat in the stream–lake pairs. All stream fishes were sampled from locations with flow rates >0·25 m s1 (i.e. riffle and run habitat types). Although stream-dwelling lepomids and rock bass are most frequently found in pool habitats (Probst et al., 1984; Schlosser, 1987), sampling in flow areas ensured that the individuals used in the study were making some use of riffles and runs (presumably for foraging). Sampling sites were between 50 and 100 m of stream channel length or lake shoreline length. Stream sites were separated from their paired lake by a distance of at least 1 km and at least one rapid or waterfall. This would make the migration of centrarchids between habitats unlikely, although some stream juveniles could have been swept downstream into the lakes. Wire funnel traps (100 cm length60 cm diameter, 1 cm mesh) were used to collect all stream samples. Lake fishes were collected from the nearshore littoral zone using a combination of funnel traps and beach seines (15·0 m1·5 m, 6 mm mesh). Physical habitat parameters from each site are described in Table II. Water velocity was measured using a hand held Pygmy Gurly current meter at a location immediately adjacent to set wire funnel traps. Vegetation density was estimated as per cent cover in a1m1 m quadrant that was randomly selected in each site. Substratum size was measured and classified according to Stanfield et al. (1996). Captured fishes were sacrificed in carbon dioxide saturated water and stored on ice for transport back to the laboratory. All fishes were frozen within 8 h of being sacrificed. Fishes were not treated with fixatives or preservatives to avoid distortions that could affect their morphological traits.
MORPHOMETRIC MEASURES Morphology of adult fishes was analysed using a modification of the box truss design (Strauss & Bookstein, 1982) that is similar to the trusses used in other studies of centrarchid morphology (Ehlinger, 1991). The truss design included 14 inter-landmark distances based on eight homologous points (Fig. 2). This method offers more complete T II. Summary of aquatic habitat parameters for the systems studied. All data were collected in May and June 1998 (see Table I for dates). Data for water velocity, water depth and water temperature are means ..(n=3). (a) Data for sites where pumpkinseed were collected. (b) Data for sites where rock bass were collected (a)
Indian River Rice Lake—unvegetated Rice Lake—vegetated
Sample size (n)963 Water velocity (ms 1 ) 0·31 0·02 0 0 Water depth (m) 0·88 0·08 1·16 0·11 0·95 0·10 Water temperature ( C) 19·6 0·2 20·0 0·0 20·0 0·0 Vegetation density <10% <10% 50–70% Dominant substratum Gravel/small cobble Gravel/small cobble Sand (0·5–1·0 mm) (10–100 mm) (10–100 mm) Mean July air temperature ( C)a 20·3 20·5 20·5 (climate station) (Trent University, (Peterborough Sewage (Peterborough Sewage Peterborough) Treatment Plant) Treatment Plant) Elevation (m) 200–210 190 190 T II. (b)
Indian River Rice Lake Eels Creek Stony Lake
Sample size (n)6666 Water velocity (ms 1 ) 0·29 0·02 0 0·36 0·05 0 Water depth (m) 0·98 0·10 1·41 0·22 1·05 0·13 1·17 0·26 Water temperature ( C) 19·5 0·2 20·5 0·2 19·0 0·4 19·3 0·3 Vegetation cover (%) <10% <10% <10% <10% Dominant substratum Gravel/small cobble Gravel/small cobble Cobble (100–300 mm) Gravel/small cobble (10–100 mm) (10–100 mm) (10–100 mm) Mean July air temperature ( C)a 20·3 20·5 19·5 19·6 (climate station) (Trent University) (Ptbo. Sewage (Apsley) (Apsley) Treatment Plant) Elevation (m) 200–210 190 245–260 240
aTaken from Environment Canada, 1993. 8 . . .
F. 2. Location of nine homologous landmarks used in the morphological analysis of pumpkinseed and rock bass (illustrated). Landmarks 1 to 8 are used to form the truss network from which the centroid was calculated. The measures include: (1-2) predorsal, (1-3) prepelvic, (1-4) preanal, (2-3) body depth, (2-4) anterior dorsal–anterior anal, (2-5) dorsal fin base, (3-4) anterior pelvic–anterior anal, (4-5) anterior anal–posterior dorsal, (4-6) anal fin base, (5-6) depth at anterior of caudal peduncle, (5-7) length of caudal peduncle (dorsal plane), (6-7) caudal peduncle truss, (6-8) length of caudal peduncle (ventral plane), (7-8) depth at posterior of caudal peduncle, (1-9) prepectoral, pectoral fin length (length of 2nd pectoral fin ray), pectoral fin width (length from end of 1st ray to end of last ray), pelvic fin length (length of 1st soft pelvic fin ray, i.e. ray next to pelvic fin spine), pelvic fin width (length from end of pelvic spine to end of last pelvic ray), dorsal fin height (length of 1st soft dorsal ray), anal fin length (length of 1st soft anal fin ray—i.e. ray next to anal fin spine), interorbital (width from orbital bone to orbital bone), width at insertion of pectoral fins (i.e. width through the body at 9 above), width at anterior of caudal peduncle (i.e. width at 5-6 above), and horizontal gape (width at the posterior terminus of the maxillary bones). coverage of the biological form of a fish, especially in terms of depth, than traditional morphometric measures (Strauss & Bookstein, 1982; Winans, 1984; Bookstein et al., 1985). As well, trusses are able to compensate for random measurement errors that may occur, and errors are more readily identified than with traditional morphometric measures (Bookstein et al., 1985). In addition, several traditional morphometric measures were used to represent the girth (width) of the fish (five measurements), fin sizes (six measurements), the position of the pectoral fins (one measurement), standard length (LS) and total length (LT). Typically, measures such as girth are not well represented in truss designs. A modified centroid was calculated from the sum of the squares of all external body measures on the fish (i.e. measurements 1-2, 1-3, 2-5, 3-4, 4-6, 5-7, 6-8 and 7-8 in Fig. 2). The modified centroid was compared to the traditional centroid measure (which includes interior measures 2-3, 4-5, and 6-7 in Fig. 2) used by other authors (Strauss & Bookstein, 1982; Ehlinger, 1991; Robinson et al., 1993, 1996). The two measures were highly correlated in all seven populations (r>0·997, P<0·0001 in all cases). All morphometric measures were taken with Ultra-Cal Mark III digital calipers (Fred. V. Fowler Co., Inc.) on the left side of fishes that were pinned to a white styrofoam background. The measurements were electronically input into a computer spreadsheet using the software ExCaliper version 2.00 (Palmer, 1994). When one of the left fins of the mid-lateral pairs was damaged, a measurement from the intact right fin was used in its place. Repeatability of the 28 morphometric measurements was determined by measuring a subsample of 15 fish a second time. The difference between the two sets of measurements was generally <5%, which is within acceptable limits for morphometric analyses (Winans, 1984). The greatest difference occurred on the width of the caudal peduncle at the insertion of the caudal fin in rock bass. This is a small measure for both species 9
(4·1–5·9 mm in rock bass; 4·1–5·4 mm in pumpkinseed). Because of the high per cent difference (8·5% in rock bass), this measure was excluded from further analyses.
DATA ANALYSIS Prior to morphometric analysis, the populations were tested for sexual dimorphism, a phenomenon that has been shown to occur in bluegill (Ehlinger, 1991). Sexual dimorphism was tested for the 25 morphometric variables using ANCOVA, with each morphometric measure as the dependent variable and the modified centroid as the covariate. All variables were first ln-transformed to linearize the relationship with the covariate. This was necessary because the modified centroid is a sum of the squares of individual linear measurements. Differences between stream and lake fishes (habitat dimorphism) were also assessed with ANCOVA. Only the 15 measures that related directly to the original hypotheses were included in this analysis. Bonferroni corrections were employed to provide a guaranteed individual probability in these multiple paired comparisons. To further examine differences among stream and lake fishes, canonical discrimi- nant function analysis (DFA) was performed on ln-transformed morphometric data. Differences in body size were removed statistically prior to running the DFA by taking the residuals from the regression of the ln-transformed morphometric variables against the ln transformed modified centroid (Ehlinger, 1991; Robinson et al., 1993; Robinson & Wilson, 1995, 1996). The residuals were used in the subsequent DFA for analysing shape independent of size. The resultant discriminant function scores were not correlated with the modified centroid or LS (r<0·01, P>0·90). To determine the separation of the samples in multivariate space, the Mahalanobis distance (D2) and associated F statistic were calculated between all pairs of samples.
RESULTS SEXUAL DIMORPHISM Significant sexual dimorphism was exhibited in 14 of 26 variables in the pumpkinseed and in 18 of 26 variables in the rock bass. Even when the probability values were Bonferroni corrected, three of the 26 variables in the pumpkinseed still showed sexual dimorphism (length of snout to anal fin, base of anal fin and interorbital width) and six of 26 variables showed sexual dimorphism in the rock bass (length of snout to anal fin, base of anal fin, interorbital width, body depth, depth of the caudal peduncle and distance between the pelvic and anal fins). Therefore, the sexes were analysed separately for habitat differences in morphology.
HABITAT DIMORPHISM (UNIVARIATE ANALYSIS) A few significant differences were found between pumpkinseeds sampled from the vegetated and unvegetated habitats in Rice Lake. In both sexes, the maximum depth of the anal fin was significantly larger, and in females, pectoral fins were significantly wider in the unvegetated sample than in the vegetated sample. The caudal peduncle was also significantly wider in females from the vegetated site relative to those from unvegetated sites. Because of these significant differences, Rice Lake pumpkinseeds from vegetated and unvegetated habitats were not pooled. Pumpkinseed of both sexes from Indian River had longer pectoral fins than those from either unvegetated or vegetated habitats in Rice Lake [supports Prediction 2; Table III(a)]. In three of the four habitat comparisons, the Indian River population had a more robust (i.e. less deep, but wider) caudal peduncle T III. Results of univariate tests (ANCOVA) for habitat dimorphism in (a) pumpkinseed, and (b) rock bass. Values are back-transformed adjusted means (mm). *Significant differences between the two populations being compared (Bonferroni corrected, P<0·0033). N/A, the ANCOVA assumption of parallel slopes was violated
Indian River v. Rice Lake unvegetated Indian River v. Rice Lake vegetated (a) Females Males Females Males Prediction Measure Indian Indian Indian Indian RL Unveg. RL Unveg. RL Veg. RL Veg. River River River River
Body depth 1 38·47* 40·21* 36·82* 37·68* 36·23 36·93 34·19* 35·52* Width at pectoral insertion 1 14·69 14·22 N/A N/A N/A N/A 13·69 13·30 Pectoral fin length 2 27·19* 25·69* 26·76* 24·31* 26·15* 24·31* 24·48* 23·20* Pectoral fin width 2 14·72 14·85 14·00 14·03 12·72 12·71 13·24 12·71 Pelvic fin length 2 17·78 17·53 16·89 17·12 16·05 15·60 16·05 15·60 Pelvic fin width 2 11·81 11·99 11·06 11·48 10·75 10·59 10·92 11·28 Anal fin length 2 14·40* 15·85* 14·04* 15·43* 13·87 14·57 13·16* 13·85* Dorsal fin height 2 14·88* 16·09* N/A N/A 14·03 14·72 13·50 14·07 Dorsal fin base 2 40·00* 38·86* 38·21 38·86 37·64 37·11 N/A N/A Anal fin base 2 17·71 17·31 17·25 16·86 17·00 16·48 15·93 15·44 Depth at anterior peduncle 3 16·15 16·59 15·39 15·91 N/A N/A 14·45* 15·27* Depth at posterior peduncle 3 11·18* 10·53* 10·53* 10·12* 9·90 9·57 9·57 9·57 Width at anterior peduncle 3 7·78* 7·01* 7·21 6·95 6·92 6·73 7·10 6·93 Prepelvic 4 34·81* 36·20* 33·58 34·09 33·15 33·62 31·69* 32·56* Prepectoral 4 27·72 27·74 27·06 26·60 25·36 25·76 25·36 25·64 T III. (b)
Indian River v. Rice Lake Eels Creek v. Stony Lake Females Males Females Males Measure Prediction Indian Indian Rice Lake Rice Lake Eels Creek Stony Lake Eels Creek Stony Lake River River
Body depth 1 46·02* 48·13* 48·33* 50·20* 42·01 41·35 40·81 40·77 Width at pectoral insertion 1 19·26 19·11 20·23 19·89 17·44* 16·79* 16·76 16·49 Pectoral fin length 2 24·63 25·15 25·23* 25·89* 22·38* 23·57* 21·89* 23·15* Pectoral fin width 2 19·28 19·73 20·21 20·55 18·19 18·69 17·83 18·12 Pelvic fin length 2 21·46* 22·51* 22·44* 23·55* 20·07 20·15 19·63 19·87 Pelvic fin width 2 14·40* 15·44* 15·30* 16·15* 13·79 13·61 13·78 13·33 Anal fin length 2 21·67* 23·31* 22·94* 24·19* 19·81 20·21 19·71 20·31 Dorsal fin height 2 22·24* 23·31* 23·78 24·24 20·05 20·15 19·73 20·01 Dorsal fin base 2 48·18 48·67 50·50* 51·16* 44·70 45·06 43·60 43·86 Anal fin base 2 29·52* 31·06* 31·41* 32·69* 27·55 27·39 26·98 27·17 Depth at anterior peduncle 3 N/A N/A 21·71 21·54 17·92 17·60 17·50 17·31 Depth at posterior peduncle 3 14·27* 14·91* 15·36 15·43 N/A N/A 13·07 13·25 Width at anterior peduncle 3 8·54 8·28 8·82 8·67 7·71 7·64 7·43 7·46 Prepelvic 4 44·52 44·84 45·88* 46·71* 40·89 41·43 39·88 40·13 Prepectoral 4 N/A N/A 41·02* 42·27* 37·04 37·26 36·42 36·53 12 . . .
(supports Prediction 3), although there were no significant differences between the Indian River and Rice Lake vegetated females. Generally, Rice Lake fish had a greater body depth (supports Prediction 1), longer anal fins (inconsistent with Prediction 2) and more posteriorly placed pelvic fins (supports Prediction 4); although these trends were not significant for the comparison of Indian River and vegetated Rice Lake females. The dorsal fin height of unvegetated Rice Lake females was greater than that of Indian River females (inconsistent with Prediction 2). In males, there was also tendency for dorsal fin height of Rice Lake pumpkinseeds to be greater than that of Indian River pumpkinseeds, but the difference was not significant in the comparison between individuals caught in the river and those caught in vegetated sites in the lake. In the comparison between river males and males caught in unvegetated sites in the lake, the regression slopes of the two groups were significantly different, but there was almost no overlap in the best-fit lines over the size range of pumpkinseeds sampled from these sites. Rock bass of both sexes sampled from Rice and Stony Lakes had longer pectoral fins than the fins of stream populations within the same sub-watershed (inconsistent with Prediction 2), although this difference was not significant for the comparison of Rice Lake and Indian River females [Table III(b)]. Rock bass from Rice Lake had longer and wider pelvic fins, longer and wider anal fins, and, for females only, taller dorsal fins than those from the Indian River (inconsistent with Prediction 2). The pectoral and pelvic fins of males were more posteriorly placed in Rice Lake (supports Prediction 4) and Rice Lake males had a greater body depth than those of the Indian River (supports Prediction 1). There were fewer significant differences between the rock bass populations of Eels Creek and Stony Lake. As noted previously, the pectoral fins of the Stony Lake fish were longer than those of the Eels Creek fish. Also, the body of stream fish at the point of the insertion of the pectoral fins was wider than that of lake fish in all four comparisons, but the difference was only significant between female rock bass in Eels Creek and Stony Lake.
HABITAT DIMORPHISM (MULTIVARIATE ANALYSIS) Significant body shape differences were detected among populations in pumpkinseeds of both sexes (females: Wilk’s =0·152, F50,120=3·8, P<0·001; males: Wilk’s =0·133, F50,148=5·2, P<0·001). With the DFA, 89% of the females and 82% of the males were correctly classified back to their a priori groups (Table IV). Indian River females were well separated in multivariate space from the females captured in unvegetated and vegetated habitats in Rice Lake (D2=12·0 and 12·5 respectively, Fig. 3). Female pumpkinseeds from these lake habitats were separated from one another to a lesser extent (D2=5·8), but the Mahalanobis distance between them was statistically significant (P=0·003). Similar results were found with the pumpkinseed males, with the river fish well separated in multivariate space from the lake fish (D2=36·1 and 25·8 in unvegetated and vegetated habitats, respectively), and the lake males from the two habitats significantly separated from one another (D2=3·7, P=0·003). Significant body shape differences were also evident in both sexes of rock bass
(females: Wilk’s =0·0697, F75,374=7·2, P<0·001; males: Wilk’s =0·0982, 13
T IV. Percentage of pumpkinseed and rock bass correctly classified to their a priori groups based on the discriminant function analysis
% correctly Sample Species Sex A priori groups classified size
Pumpkinseed Females Indian River 92·3 26 Unvegetated 81·8 33 Vegetated 92·9 28 Pooled females 88·5 87 Males Indian River 100 14 Unvegetated 81·6 49 Vegetated 76·3 38 Pooled males 82·2 101 Rock Bass Females Indian River 91·4 35 Rice Lake 92·7 41 Eels Creek 84·6 39 Stony Lake 92·1 38 Pooled females 90·2 153 Males Indian River 86·1 36 Rice Lake 90·0 40 Eels Creek 85·4 41 Stony Lake 76·9 26 Pooled males 85·3 143
F75,344=5·4, P<0·001). The DFA was able to correctly classify 90% of the females and 85% of the males in the four waterbodies (Table IV). Females and males from all of these populations were separated by significant Mahalanobis distances (Fig. 4), with the Indian River–Rice Lake pair more widely separated than the Eels Creek–Stony Lake pair (females: D2=14·2 and 5·3; males: D2=18·7 and 4·8, respectively).
DISCUSSION Morphological differences between stream and lake fish were evident in both pumpkinseeds and rock bass, though they were not always consistent among populations or species. Stream–lake differences in body form were evident from the DFA, despite some overlap among the populations (Figs 3 and 4). The degree of overlap on the canonical axes and the few fish at the extreme ends of the axes suggest that pumpkinseed and rock bass do not fall into two discrete categories (i.e. a discrete stream morph and a discrete lake morph). A lack of discrete morphological types was also found by Robinson & Wilson (1996) in their study of trophic dimorphism in pumpkinseeds. They found that pumpkin- seeds formed a unimodal distribution of pelagic and littoral morphs, and that the general body shape of most individual fish was located at an inter- mediate position on this distribution somewhere between the extreme pelagic and the extreme littoral forms. Robinson et al. (1993, 1996) correctly assigned 14 . . .
5 (a)
0 Axis 2
–5 –5 05
4 (b)
0 Axis 2
–4 –7 07 Axis 1 F. 3. Distribution of (a) pumpkinseed female and (b) pumpkinseed male canonical scores from the discriminant function analysis (DFA) with 50% ellipsoids about the centroid of each group plotted on the first two canonical axes. The DFA was performed on the residuals after regressing each of the morphological variables against the centroid developed from the truss network shown in Fig. 2. Pumpkinseeds collected from the Indian River (), Rice Lake unvegetated habitat ()and Rice Lake vegetated habitat (). pumpkinseeds to their trophic group 81–89% of the time with DFA. Similarly, 82–90% of the present fishes were correctly classified to their a priori group by the same statistical technique. Prediction 1, that stream fishes would be more slender-bodied than lake fishes, was generally supported by this study. In both species, the body was less deep in the stream populations, but in most comparisons, there was no significant difference between stream and lake populations in width through the body. The stream–lake differences in body depth are consistent with the findings of other morphological studies. Fishes inhabiting ecosystems with more arduous hydro- dynamic conditions, such as streams, tend to be more slender-bodied to reduce the drag induced by the current (Webb, 1984; McLaughlin & Grant, 1994; Ryder & Pesendorfer, 1989). Fishes with a more gibbose body shape suffer higher drag penalties when swimming. Bronmark & Miner (1992) found that crucian carp Carassius carassius (L.) with deeper bodies had a 32% increase in drag at a 15
5 (a)
0
–5 –6 06 Axis 2 5 (b)
0
–5 –5 05 Axis 1 F. 4. Distribution of (a) rock bass female and (b) rock bass male canonical axis scores from the discriminant function analysis (DFA) with 50% ellipsoids about the centroid of each group plotted on the first two canonical axes. The DFA was performed on the residuals after regressing each of the morphological variables against the centroid developed from the truss network shown in Fig. 2. Rock bass collected from the Indian River (), Rice Lake (), Eels Creek ( ) and Stony Lake (). swimming speed of 10 cm s1 in small ponds. The added drag penalty would decrease the swimming performance of the fish, but minimization of resistance does not appear to be important in the type of low-speed manoeuvring performed by fishes that forage in complex lake environments (Webb, 1998). With the increased burden of swimming in the stream due to the hydro- dynamic conditions, selection pressures should favour the development of mechanisms that allow sustained swimming to be maintained. Fishes selected for sustained swimming ability are generally more slender-bodied, rounder in cross-section and have a greater proportion of red muscle tissue, whereas more 16 . . . sedentary lake fishes are generally more gibbose, more laterally compressed (or oblong in cross-section) and have a higher percentage of white muscle tissue (Ryder & Pesendorfer, 1989). The use of current refuges in the stream (e.g. boulders or submerged logs) may allow the fish to reduce its need for unsteady swimming and allow it to maintain its position with steady swimming at a slower rate. In laboratory tests, steady swimming was two to four times less energetically costly than unsteady swim- ming (Webb, 1991), so this type of locomotion should be favoured. Similarly, in field situations, the use of even small-scale current refuges reduced swimming costs in brook trout by 10% on average, while foraging ability was not affected (McLaughlin & Noakes, 1998). The use of such habitat structure provided individuals with an energetic advantage. Pumpkinseed and rock bass inhabiting streams undoubtedly use such refuges and backwater areas to reduce swimming costs. It is likely that stream centrarchids only utilize the faster flowing water when they are feeding on invertebrates caught drifting in the current, and this feeding would occur from sheltered locations whenever possible. Contrary to Prediction 1, stream and lake fishes generally did not show a significant difference in body width. While this dimension has not been measured in most previous studies of morphological differences in flowing waters (Bodaly, 1979; Baltz & Moyle, 1981; Beacham et al., 1989; McLaughlin & Grant, 1994), it was expected that having a reduced body depth might have an influence on the body width of the fish. According to Ryder & Pesendorfer (1989), more fusiform fishes are typically rounder in cross-section than gibbose fishes. A rounder cross-section, however, can be generated by a reduction in body depth, without necessarily increasing body width. Prediction 2, that stream fishes will have longer and wider fins, was not supported. It was expected that stream centrarchids would have larger paired lateral fins for holding position and for orientating themselves in the current, and that larger dorsal and anal fins would be used for stability in flowing water. While stream pumpkinseed pectoral fins were longer than those of lake pump- kinseed, in most other cases the length and width of the fins was greater in the lake fish. Anal and dorsal fin heights were greater in lake fishes of both species, and all fin sizes (pectoral, pelvic, anal and dorsal) were larger in the lake dwelling rock bass. According to Webb (1984), fishes adapted to prolonged steady swimming should have a larger fin area relative to body size. Chinook salmon Oncorhynchus tshawytscha (Walbaum) inhabiting areas with faster current velocities did have larger lateral fins (Beacham et al., 1989). Brook charr use their fins to maintain an upstream orientation in the faster, often turbulent flow (McLaughlin & Noakes, 1998). Larger fins should move a greater volume of water and may reduce energy expenditures from additional fin beats. In addition, larger fins may be used by stream fishes in conjunction with steady swimming, a propulsive mechanism observed for stream fishes in the field (Webb, 1991; McLaughlin & Noakes, 1998). The dorsal and anal fins of stream-dwelling coho salmon are larger than those of lake-dwelling coho, although this may be due to increased territorial behaviour in the stream (Swain & Holtby, 1989). Territorial fishes use larger dorsal and anal fin margins to create the illusion of increased body size. 17
Larger fins can create a greater drag potential in flowing water. The use of lateral fins increases the surface area of the fish when it is viewed head-on. If a fish is oriented in an upstream direction to forage on aquatic insects drifting in the current, the increase in surface area exposed to the current would result in a greater drag coefficient. This would reduce the distance covered per tail beat, or alternatively, it would mean that a fish would have to increase its tail beat frequency to hold position in the current (Webb, 1991; McLaughlin & Noakes, 1998). Similarly, an increase in the surface area of the dorsal and anal fins would be sub-optimal when a fish is not oriented precisely in an upstream direction, as the fins would catch the current as a sail catches the wind. Optimal fin size may be a trade-off between the use of large fins for orientation and maintaining position, against the extra drag that is created by these larger fins. The optimal solution to this trade-off may vary in species that differ in overall body shape, or which use the fast current of a stream to a different degree. Prediction 3, that stream fishes will have a more robust caudal peduncle than lake fishes (reduced depth but greater width), was partly supported. In pump- kinseed, stream fish had a more shallow depth at the anterior end of the caudal peduncle (although this difference was only significant for males) and stream fish had a wider caudal peduncle (although this result was only significant for females). There were few significant differences, however, in the width or depth of the caudal peduncle in rock bass. For prolonged, constant speed swimming, stream fishes require a caudal peduncle that is muscular, yet capable of large amplitude beats to increase the forward thrust power of the fishes (Webb, 1984). To allow for faster, more powerful swimming, stream fishes also need to be able to make these large amplitude caudal peduncle displacements at high frequencies. A shallow caudal peduncle with a large muscle mass (i.e. increased width) allows the fish to maximize thrust while reducing energy lost in recoil (Webb, 1984, 1998; McLaughlin & Noakes, 1998). McLaughlin & Grant (1994) found that juvenile brook charr collected from sites with faster current had a shallower caudal peduncle than those collected from sites in the same watershed with a slower current velocity. Although the width of the caudal peduncle was not measured by McLaughlin & Grant (1994), it would probably be greater in stream fish to contain the increased muscle mass necessary for prolonged steady swimming (Webb, 1984). It is curious that in the present study, the depth of the anterior caudal peduncle was smaller in stream fishes, whereas the depth at the posterior of the caudal peduncle was greater than that of lake fishes. While it was expected that the entire caudal peduncle would be less deep in stream fishes, energy losses in recoil would be reduced as long as the lateral surface area of the caudal peduncle is smaller in a relative sense. The posterior depth of the caudal peduncle was measured from the dorsal insertion of the caudal fin to the ventral insertion of the caudal fin. If the base of the caudal fin was larger in stream fishes, then the depth of the caudal peduncle at the insertion of the fin would also be greater. Although caudal fin dimensions were not measured in the current study, McLaughlin & Grant (1994) report that brook charr captured from faster flowing water had larger caudal fins. 18 . . .
Prediction 4, that the lateral fins of stream fishes would have a more anterior placement than in lake fishes was partly supported. In the pumpkinseed, the pelvic fins of both sexes were more anterior in stream populations, but the pectoral fins were not. In the rock bass, both the pelvic and the pectoral fins were generally more anterior in stream populations, but this result was only significant for males in one of the two habitat comparisons. Although published data on the placement of the lateral fins are sparse, there is some evidence that the pectoral and pelvic fins of stream fishes are located in a more anterior position than those of lake fishes (Swain & Holtby, 1989). The more anterior insertion of the lateral fins allows for additional manoeuvrability in fishes (Webb, 1984), an adaptation that is necessary for stream fishes that must orient and maintain their position in flowing water. It is evident from the above discussion that the observed morphological differences in the current study were not always consistent between the two species studied, nor were the observed results always consistent with other studies. Although the results for many of the variables were consistent between the two species (i.e. if for a certain trait, stream pumpkinseed were larger than lake pumpkinseed, then stream rock bass would also be larger than lake rock bass), there were a few exceptions. For example, the length of the pectoral fins and the length of the dorsal fin base were greater in stream pumpkinseed and in lake rock bass. There are a number of examples of conflicting results in the literature. For example, Bodaly (1979) found two morphological forms of lake whitefish Coregonus clupeaformis (L.), a benthic morph and a pelagic morph, in five different Yukon lakes. Although the two morphs could be consistently distin- guished within a single lake, the sets of differences that distinguished them were not consistent among the five lakes. Bodaly (1979) suggested that the among-lake differences might have occurred because the fish were not only adapting to the two niches available in each lake, but also to environmental differences that exist among the lakes. Similar mechanisms may be influencing the morphology of the fishes in the present study. One question that cannot be answered from the study is whether the observed morphological differences between stream and lake populations are the result of genetic differentiation or phenotypic plasticity. Evidence from stream–lake studies of other species and from studies of pumpkinseed differentiation in lakes suggest that both mechanisms may contribute to stream–lake differentiation in pumpkinseed morphology. In threespine stickleback evidence from rearing studies indicates that the morphological traits of stream and lake morphs are inherited (Lavin & McPhail, 1993), and subsequent mtDNA analysis of popula- tions from a stream and an adjacent lake indicate that the gene pools of the two are distinct (Thompson et al., 1997). Similarly, juvenile coho salmon from a lake and an adjoining stream showed differences in body depth, fin placement and colouration even after 2 months of rearing in a common environment (Swain & Holtby, 1989). In contrast, the variation in juvenile brook charr body depth, caudal peduncle depth and caudal fin height between individuals inhabiting slow and fast flowing sites within a stream appears to be due mainly to phenotypic plasticity, as the morphological differences apparent in one year did not persist several years later (Imre et al., 2001). Furthermore, in a rearing experiment with 19 littoral and pelagic forms of one of the test species, Robinson & Wilson (1996) estimated that 53% of the observed dimorphism in pumpkinseeds was attributable to phenotypic plasticity, whereas genetic differences accounted for only 14% of the variation. A combination of genetic analysis and controlled rearing experiments would be required to identify the relative importance of phenotypic plasticity and divergent selection.
We wish to thank M. Allen, S. Bobrowicz, S. Bowman, K. Brodribb, K. Caldwell, M. Duffy, L. Gatzke, K. Ovens, A. Todd, V. Vaughan and M. Wilson for their assistance in the field. As well, thanks are extended to B. Robinson and K. Somers for their helpful advice during this study, and to N. Mandrak and T. Whillans for their advice and comments on an earlier version of the manuscript. Financial support for this study was provided by a Natural Sciences and Engineering Research Council of Canada grant to M. Fox and an Ontario Graduate Scholarship to J. Brinsmead.
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