ECOLOGY OF UPPER KLAMATH LAKE SHORTNOSE AND LOST RIVER SUCKERS
4. The Klamath Basin sucker species complex
1999 ANNUAL REPORT (partial)
SUBMITTED TO U. S. Biological Resources Division US Geological Survey 104 Nash Hall Oregon State University Corvallis, Oregon 97331-3803 & Klamath Project U. S. Bureau of Reclamation 6600 Washburn Way Klamath Falls, OR 97603 by Douglas F. ~arkle', Martin R. ~avalluzzi~,Thomas E. owli in^^ and David .Simon1
1Oregon Cooperative Research Unit 104 Nash Hall Department of Fisheries and Wildlife Oregon State University Corvallis, Oregon 97331-3803 E -mai1 : douglas.markle@,orst.edu
2Department of Biology Arizona State University Tempe, AZ 85287-1501 Phone: 480-965-1626 Fax: 480-965-2519 E -mai 1 : [email protected]
July 26, 2000 There are 13 genera and 68 species of catostomids
(Nelson 1994) with three genera and four species occurring in Klamath Basin (Bond 1994)- Catostomus rimiculus Gilbert and Snyder, 1898 (Klamath smallscale sucker, KSS), C. snyderi Gilbert 1898 (Klamath largescale sucker, KLS),
Chasmistes brevirostris Cope, 1879 (shortnose sucker, SNS), and Deltistes luxatus (Cope, 1879) (Lost River sucker,
LRS). Lost River and shortnose suckers are federally listed endangered species (U.S. Fish and Wildlife Service 1988).
The four Klamath Basin suckers are similar in overall body shape, but highly variable, and are distinguished by feeding-related structures, adult habitat and geography.
The two Catostomus species have large lips, widely-spaced gillrakers, and are primarily river dwellers with C. snyderi mostly found in the upper basin and C. rimiculus in the lower basin and adjacent Rogue River. Deltistes luxatus has smaller lips, short "deltoid" Catostomus-like gillrakers, and is primariliy a lake dweller. Chasmistes brevirostris has small lips, many closely-spaced gillrakers with secondary branching, and is also primarily a lake dweller (Andreasen 1975, Miller and Smith 1981, Buettner and Scoppettone 1991).
Catostomids were among the first freshwater fish known to hybridize in nature (Hubbs, et al., 1943). Miller and Smith (1981) stated they "had not seen any recently- collected specimens from (Upper) Klamath Lake that are the same as brevirostris", that the traits indicated introgression with C. snyderi, and that 'none of the available names is applicable" to Klamath Basin populations. This and other problems with species identification prompted a morphological and genetic study of Klamath Basin suckers. The objectives were to understand sources of variation, provide field biologists with usable identification criteria, and provide initial identifications for a multi-investigator sucker genetics program, referred to herein as KLAMGEN.
STUDYAREA
The KLAMGEN specimens were collected from the Klamath and Rogue river basins in south central Oregon and northern
California (Fig. 1). Klamath Basin collections targetted five subbasins (Fig. 1). The Upper Williamson subbasin is that part of the Williamson R. above Klamath Marsh. The
Sprague subbasin is the Sprague R. above Chiloquin Dam including the Sycan R. Specimens caught in the ladder at
Chiloquin Dam were considered to be in the Sprague subbasin. Upper Klamath subbasin includes Upper Klamath
Lake, the lower Williamson R., lower Sprague R. downstream of Chiloquin Dam, and the Link River downstream of Klamath Falls. The Lost River subbasin includes Clear Lake, Lower
Klamath Lake and Gerber Reservoir. The Lower Klamath subbasin includes the three downstream reservoirs (J. C.
Boyle, Copco, and Iron Gate) and Jenny Cr. Specimens collected outside the KLAMGEN program were also assigned to the appropriate subbasin. See U.S. Department of the
Interior, Bureau of Land Management (1995) for detailed descriptions of the climate, geology, and topology of the
Klamath Basin.
MATERIALSAND METHODS
Abbreviations for museum acronyms follow Leviton -et
-al. (1985). We examined 1782 suckers - 1741 from the Klamath Basin and 41 from the Rogue River. The most extensive data collection was on 333 adult specimens collected for the KLAMGEN project (Table I), of which 325 carcasses were deposited in the Oregon State University
Fish Collection (0s). Eight specimens were sampled non- lethally for tissues. The KLAMGEN protocol attempted to obtain samples from suspected spawning groups in spring and early summer, 1993-1994, but 183 (55%) were collected outside the spawning seasons in August-November 1993. Much additional Klamath material (1085 specimens) was obtained from juvenile collections (Markle and Simon unpublished), also deposited at OS and radiographs of the holotype of C. brevirostrisi (ANSP 20950), holotype of Ch. stomias (USNM
48223, and holotype of Ch. copei USNM 48224. Unless noted all analyses are based on the entire data set.
Abbreviations and descriptions of counts and measurements are found in Table 2 and generally follow
Hubbs and Lagler (1964). All vertebral and vertical fin ray counts were taken from radiographs and do not include the four Weberian centra. All measurements were in mm. Lip area and perimeter were calculated for 32 specimens using a digital imagery system equipped with Optimas 5.0 (1995) software. Not all variables were measured for all specimens because of damage or lack of variation detected after preliminary analyses.
Data were analyzed using STATGRAPHICS Plus (1994-
1996). Univariate characters were evaluated using Kruskal-
Wallis non-parametric ANOVA to test for significant differences with comparisons adjusted using the Bonferroni inequality. Multivariate analyses used Principle
Components Analyses (PCA) to reduce data and uncover data structure and Discriminant Functions Analysis (DFA) to classify individuals.
DNA was extracted from 324 KLAMGEN individuals and initially screened with several sets of primers from the cytochrome b and ND4L genes. Those that amplify the ND4L gene were selected because of ease of scoring and sequencing. Sixteen haplotypes were identified from 324 individuals (Table 1) . RESULTS
Lip morphology and initial identification. ---Initial field identifications of C. snyderi and Ch. brevirostris were inconsistent. In Upper Klamath, Sprague, and Upper
Williamson subbasins both species were identified based on overall appearance, primarily lip morphology, whereas a single species (Ch. brevirostris) was identified in the field in Lost River subbasin. We surveyed our quantitative and categorical lip morphology characters (below) and re- identified Lost River Ch. brevirostris as C. snyderi if the following combination of characters was present in an individual:
1) symphyseal lower lip gap absent, teratological, or
present anteriorly but lips touch posteriorly
(LLGAP= N, T or A) , and
2) length of contact of lower lip lobes greater than
50% of eye diameter (GAPLMM/EYE>o.5) . All subsequent analyses are based on these identifications and all descriptions of lip morphology are based on KLAMGEN specimens. Lips of Catostomus species were larger with more surface area relative to the lip perimeter than lips of D. luxatus or Ch. brevirostris (Fig. 2) . Based on a Bonferroni multiple range test, the means of the AOMMM/POMMM ratio sorted into two significantly different homogenous groups,
Catostomus species and D. luxatus plus Ch. brevirostris.
The position of the posterior margin of the lower lip
(LLLRM) was scored as anteriad, even or posteriad of the ventroposterior corner of the maxilla (Fig. 3). Specimens with small lips ending anteriad of the maxilla also had a short distance between the symphysis of lower jaw and the point where lower lip lobes separate (GAPLMM) (Fig. 4).
Specimens with larger lips extending posteriad of the maxilla had larger GAPLMM while those with lips even with the maxilla were bimodal for this character (Fig. 4).
Expressed as a ratio to eye diameter, the GAPLMM measurement fell into two categories, less than or greater than 50% (Fig. 4). Lips were posteriad of the end of the maxilla in 100% of C. rimiculus, even or posteriad of the maxilla in 98.9% of C. snyderi, even or anteriad of the maxilla in 95.6% of Ch. brevirostris, and anteriad of the maxilla in 100% of D. luxatus.
The presence or absence of a symphyseal gap between the lobes of the lower lip (Fig. 3) was also related to the GAPLMM/EYE ratio in specimens (Fig. 5). When a gap is present, the ratio is smaller. Again, the GAPLMM measurement fell into two categories, less than or greater than 50% of the eye diameter (Fig. 5). Catostomus species generally had no lower lip gap, but 9.1% of C. rimiculus
(n=55) and 8.4% of C. snyderi (n=95) had lower lip gaps. In
Ch. brevirostris, 100% of Sprague and Upper Klamath specimens possessed a lower lip gap and 72.7% of Lost River specimens had a lower lip gap. All specimens of D. luxatus had a lower lip gap. The lower lip gap developes early and
is present in young-of-the year juveniles (Fig. 6). In 103
Ch. brevirostris 27.9-90.2 mm SL from Upper Klamath Lake
(0s 13969 & 13982), two lacked a lower lip gap while all 51
C. snyderi from the Upper Williamson R. (0s 13882) lacked a
lower lip gap.
Lip and lower jaw deformities complicate
interpretation of these structures. Two Upper Williamson C.
snyderi had incomplete development of the branchiostegal membranes creating a long gap extending from the isthmus to the symphysis of the lower jaw (0s 015903-A, B). Other
specimens had distorted jaws and lips which we attributed to fixation, but which could be deformities.
DNA.---Most haplotypes (n=10) were rare, occurring in only one or two individuals, while the remaining six haplotypes were found in at least 12 individuals (Table 3, Fig. 7) .
Individuals of C. rimiculus always exhibited haplotypes 'I" in Klamath Basin and haplotype 'L" in the Rogue R. and only
'I" was found in other species. Each C. rimiculus haplotype was more similar to the common haplotype of D. luxatus than to each other. Most D. luxatus (33 of 40) had haplotype
"K" that was rarely found in other species. Haplotype 'N", that appears to be derived from haplotype 'K", was more common in Ch. brevirostris (7) than in C. snyderi (3) or D. luxatus (2). Both C. snyderi and Ch. brevirostris, had high frequencies of the 'B" haplotype, however, 17 Upper
Williamson R. C. snyderi had haplotype 'F" that was found nowhere else.
Meristics.---A subset of 135 KLAMGEN individuals were examined using PCA for 20 characters (characters listed in
Table 2, excluding nasal lamellae, infraorbital pores anterior to eye, and gill rakers on medial surface of first gill arch). Groups of similar counts were highly
significantly correlated. All scale counts had Spearman
rank correlations from 0.34-0.94 and peO.OOO1; and all
lateralis pore counts had Spearman rank correlations from
0.35-0.74 and peO.OOO1. No sexual dimorphism was detected
in the first four componenets (Kruskal-Wallistest of medians p=0.14-0.99), although number of gillrakers was significantly higher (p=O.005) in male C.rimiculus (x=25.7,
N=16) than in females (x=24.7, N=38).
Based on the entire data set, numbers of gillrakers
(GILRKRANT) on the first arch had a strong ontogenetic or
size signal (Fig. 8) . The relationship for each species was expressed as, Gill rakers=A + B/SL. The coefficients, r2 and
sample sizes (n) were:
KSS - A=26.1, B=-365, r2 =32.3, n=64;
LRS - A=29.4, B=-291, r2 =53.9, n=201;
KLS - A=35.1, B=-371, r2 =72.3, n=257 and;
SNS - A=39.9, B=-453, r2 =58.0, n=565 (Fig. 9).
All species approach an asymptote at about 200 mm SL (Fig.
9) with the predicted number of gill rakers, progressing
from a low of 26.1 in KSS to a high of 39.6 in SNS. The
size and gill raker count of 28 nominally "pure" Ch.
brevirostris reported by Miller and Smith (1981) are
illustrated by the box in Fig. 9. Because 95% of the
KLAMGEN specimens were > 200 mm SL, we did not correct for
this bias in the PCA.
A reduced subset of five characters (INFORBPOR,
GILRKRANT, LLSCALES, PAPUPRLIP, and VAO) with complete data
for 186 KLAMGEN specimens provided species discrimination
similar to the full dataset (Fig. 10). The first two axes
accounted for 46.2% and 28.9% of the variance in the data set. Haplotype data were mapped onto the factor score patterns. The common "I" haplotype of Klamath C. rimiculus
was also found in D. luxatus (Fig. 11). The common 'K"
haplotype of D. luxatus was found in Ch. brevirostris, most
of which had positive PC I1 scores (Fig. 11). Ch.
brevirostris and C. snyderi shared the 'B" haplotype that
was also found in three D. luxatus (Fig. 11).
Overall Morphology.---The head and lip morphology are
partly the basis for initial identification and two ratios
(GAPLMM/EYE and LAE/HD) result in four distinct morphotypes
(Fig. 12). The species tend to fall into long-snouted (D.
luxatus and C. rimiculus) or short-snouted (C. snyderi and
Ch. brevirostrisi) forms and big-lip (C. rimiculus and C.
snyderi) or small-lip (D. luxatus and Ch. brevirostris)
forms (Fig. 12). Haplotype data for these fish indicate
that the common "B" haplotype of Ch. brevirostris and C.
snyderi was also found in three D. luxatus and one C.
rimiculus (Fig. 13A). All four of these hybrids have the
maternal morphology for these characters. The common 'K"
haplotype of D. luxatus is found in five Ch. brevirostris
and one C. snyderi (Fig. 13B) . Four of these presumed
hybrids had the paternal morphology for these characters.
Males generally had longer pectoral fins and females
generally had longer pre-anal lengths so the ratio of LP~/LOAwas larger (25.4%) in males than females (23.7%) and means significantly different (p<0.001) in all species except D. luxatus.
Twenty nine morphological characters of Table 2 were linearly regressed on standard length for a subset of 109
KLAMGEN individuals and the residuals used in a PCA. Lost
River subbasin specimens were excluded. Characters with loadings less than 0.3 on the first two factors were sequentially removed resulting in a subset of 10 characters. Characters considered redundant measures of the same feature, such as those of the lips, and which had similar loadings on both axes were reduced to the feature with the maximum discrimination power. The resulting five characters (HL, DDO, GAPLMM, LAE and LOD) discriminated characters in a manner similar to the set of 29 (Fig. 14).
The two axes accounted for 45.8% and 33.2% of the variance in the data and provide modest separation of species. The first axis primarily reflects differences in head, snout and predorsal lengths and most specimens with negative scores are Sprague R. C. snyderi. In fact, C. snyderi spans the entire range of variation in the first axis. C. rimiculus had high scores on both axes reflecting its large lips, long snout, and shallow body depth. Both Ch. brevirostris and D. luxatus had low PC I1 scores reflecting
their small lip size.
Head length was examined further and, as a proportion
of SL, decreased with size. For 795 Klamath Basin suckers
representing all species the correlation coefficient was - 0.59 (~~=35-4%). In Ch. brevirostris, the correlation
coefficient was -0.62 (~~=38.9%)(Fig. 15). Type material of
four nominally "pure" Ch. brevirostris reported by Miller
and Smith (1981) have larger heads for their size than our
material.
Cd TOSTOMUS R IMICULUS
Description.---Body elongate with trunk tending towards a
uniform height(Fi.9. 16 & Fig. 14); caudal peduncle
relatively deep, 60-71% head depth; snout angular and long
(Fig. 14); lips large, fleshy, papillose; lower lip lobes
quite large, extending well posteriad of ventroposterior
corner of maxilla, and in contact along midline for a
distance greater than 50% of eye diameter; gill rakers 22-
27 in adults>200 mm SL and reaching adult modal count of
26.1, widely-spaced with simple ridges and relatively
little secondary branching; 41-45 post-Weberian vertebrae;
mean size of KLAMGEN females larger (371 mm SL, n=37) than
males (309 mm SL, n=17); number of gillrakers significantly higher (p=0.005) in males (x=25.7, N=16) than females
(~=24.7,N=38) . Geographic variation.---The dorsal fin was further back in C. rimiculus from the Rogue Basin (Fig. 16) . This feature was reflected in fewer caudal vertebrae (Rogue mean=18.7, n=30 vs. Klamath mean=19.7, n=25), more vertebrae in front of the dorsal fin origin (Rogue mean=15.0, n=30 vs. Klamath mean=13.7, n=25), and a higher LOD/SL ratio (Rogue mean=49.2%, n=30 vs. Klamath mean=47.8%, n=25). All differences were significant (p<0.001). In addition, all C. rimiculus from the Rogue R. had ND4L haplotype 'L" while all from the Klamath had haplotype 'I".
Hybridization.---TheKLAMGEN samples give evidence of hybridization with D. luxatus (0s 15920 B&C, OS 15929 C) and C. snyderi (Fig. 17, OS 15906 B, OS 17476 A) based on the presence of the 'I" haplotype in specimens morphologically fitting these species(Fig. 10). However, two of these nominal "hybrids" were found in the Lost River subbasin where C. rimiculus has never been found and a third was found in Upper Klamath Lake where only one C. rimiculus has ever been found. These data suggest C. rimiculus is present but rare in both subbasins, a situation conducive to hybridization. Miller and Smith
(1981) identify nominal hybrids with Ch. brevirostris from Copco reservoir, primarily based on co-occurrence
("Catostomus rimiculus is common in the reservoir").
Comments.---Our range for gill rakers in Klamath C. rimiculus, 22-27, is considerably narrower and the average lower than the range for 12 Copco Reservoir specimens (22-
33) reported by Miller and Smith (1981). They also reported
34 nominal hybrid C. rimiculus X Ch. brevirostris from
Copco with a range of 33-48 gill rakers. Our KLAMGEN samples from Copco contained 11 Ch. brevirostris and one C. rimiculus and no indication of hybridization, although we do find evidence of C. rimiculus hybridization elsewhere
The upstream reservoir, J. C. Boyle ("Topsy"), produced more C. rimiculus (24) for the KLAMGEN study. More recent work in 1998 and 1999 confirms the pattern that adult C.
rimiculus are more abundant in the reservoir closest to
Upper Klamath Lake (J. C. Boyle) and adult Ch. brevirostris are more abundant, by about 10:1, downstream in Copco
(Desjardins and Markle, unpublished). The recent work also provides no evidence of self-sustaining populations of Ch. brevirostris in Copco, thus suggesting that Ch. brevirostris in Copco dispersed downstream from Upper
Klamath Lake, a conclusion consistent with our study.
DELTISTES LUXATUS Description.---Bodyelongate with trunk tending towards a uniform height or rising to the dorsal base(Fig. 18, Fig.
14); caudal peduncle depth relatively shallow, 40-66% head depth; adults large up to 1 m; snout angular and long (Fig.
14); lips small; lower lip lobes with a gap present and ending anteriad of ventroposterior corner of maxilla; gill rakers 26-34 in adults>200 mm SL and reaching adult modal count of 29.4; 44-48 post-Weberian vertebrae; mean size of
KLAMGEN males (453 mm SL, n=21) larger than females (398 mm
SL, n=21).
Geographic variation. - - -D. luxa tus from Lost River subbasin averaged significantly more vertebrae than those from Upper
Klamath Lake (46.1, n=17 vs.44.9, n=26; p=0.0001); significantly more cephalic pores, for example, more infraorbital pores (38.1, n=16 vs. 30.6, n=25; p=0.0001); and significantly smaller scales, for example, more lateral line scales (90.4, n=16 vs. 85.4, n=25; p=0.01). Although
Lost River subbasin fish were also larger (460 mm SL vs.
395 mm SL) these characters are not known to change ontogenetically and are suspected as indicating geographic differences.
Hybridization. ---The KLAMGEN data indicate that D. luxatus hybridize with all other species in the Klamath Basin (Fig.
18) - with C. snyderi (0s l59l5B), with C. rimiculus (0s 15920 B&C, OS 15929'2) and with Ch. brevirostris (0s 15924C,
OS 15926, OS 15929B, OS 15953B, OS 15961A, OS 17479 and OS
17480). Two related haplotypes ("Nu and '0") appear derived from the "K" haplotype of D. luxatus (Fig. 19) but have the curious pattern of being found in the Upper Klamath subbasin only in three D. luxatus and in the Lost River subbasin in seven Ch. brevirostris and three C. snyderi.
Assuming the K->N mutation arose in D. luxatus, this pattern is consistent with back-crossing and retention of the D. luxatus haplotype in otherwise normal Ch. breviros tri s and C. snyderi .
Comments.---Populationsof D. luxatus are known from the
Sprague subbasin but have been unavailable for study. The relatively strong meristic differentiation of Lost River and Upper Klamath specimens suggests that D. luxatus spawning in the Sprague R. above Chiloquin Dam might also show geographic differences. Based on the ND4L gene, D. luxatus may play a central role in Klamath Basin sucker taxonomy. The gene indicates evidence of crossing with all four species, including six specimens of other species with the "K" haplotype, evidence of independent derivation of C. rimiculus haplotypes 'I" and 'L" from the 'Kw haplotype, and evidence of introgression of D. luxatus mitochondria1
DNA in two other species. CATOSTOMUSSNYDERI
Description.---Body moderately deep (Fig. 20) ; caudal peduncle depth relatively shallow, 47-66% head depth; snout rounded and short(Fig. 14); lips large papillose and ending posteriad (68%), even (13%) or anteriad (18%) of ventroposterior corner of maxilla, gap absent in 93%; gill rakers 29-40 in adults>200 mm SL and reaching adult modal count of 35.1; 40-46 post-Weberian vertebrae (97.5% 42-44); mean size of KLAMGEN females larger (366 mm SL, n=49) than males (320 mm SL, n=48).
Geographic variation. - - - Some regional differentiation was apparent in a PCA of five meristic characters (Fig. 21) with specimens from the Lost River subbasin tending to have fewer upper lip papillae. Within Williamson drainage C. snyderi, the head length-size relationship differs between subbasins (Fig. 24). Fish from the Upper Williamson above
Klamath Marsh have larger heads than fish from the Sprague
R. (Fig. 20). Lost River C. snyderi are intermediate; for fish > 300 mm SL, the average HL/SL ratios are 0.25 (Upper
Williamson, n=l6), 0.24 (Lost River, n=25), and 0.23
(Sprague, n=22) and a Bonferroni multiple range test showed significant differences (p=0.0001). Haplotype 'F" was restricted to Upper Williamson subbasin. Hybridization. - - -The KLAMGEN specimens indicate hybridization with C. rimiculus (Fig. 17) (0s 15906 B, OS
17476 A) and D. luxatus (0s 15915B) (Fig. 18). The absence of a mitochondria1 marker precludes discovery of hybridization with Ch. brevirostris, but we believe it takes place.
Comments. - - -The large-headed, 'F" haplotype C. snyderi of the Upper Williamson deserve more study. Currently, the only species known to be endemic to upper tributaries of the Williamson and Sprague (Sycan) rivers is Lampetra minima (Lorion et al., 2000). The differentiation seen in
C. snyderi from the Upper Williamson may reflect a common pattern of isolation of these upper tributaries.
CHASMISTES BREVIROSTRIS
Description.---Body moderately elongate generally rising towards dorsal (Fig. 22) ; caudal peduncle depth relatively shallow, 44-68% head depth; lips small and ending posteriad
(2%), even (28%) or anteriad (70%) of ventroposterior corner of maxilla, gap present in 98%; gill rakers 30-46 in adults>200 mm SL and reaching adult modal count of 39.9;
41-45 post-Weberian vertebrae; mean size of KLAMGEN females larger (348 mm SL, n=56) than males (318 mm SL, n=58);
Geographic variation. ---Some regional differentiation was apparent in a PCA of five meristic characters (Fig. 23) with specimens from the Lost River subbasin tending to have higher infraorbital pore counts (p=0.06). Specimens from lower Klamath R. reservoirs resembled those from Upper
Klamath Lake (Fig. 23). These differences were more obvious in a bivariate plot of gill rakers and lateral line scales using all available specimens (Fig. 21).
Hybridization.---See above under D. luxatus and C. snyderi.
Comments.--- The greatest overlap in morphological characters occurs between C. snyderi and Ch. brevirostrisi
(Figs. 10-14). In addition, these species share a common
ND4L haplotype, 'B". These species are readily distinguished by lip morphology (Fig. 12), have different ontogenetic trends in gill raker counts (Fig. 81, and different geographic distributions, though they are sympatric in the Lost River and Upper Klamath plus Sprague subbasins. DISCUSSION
Considering their current classification in three genera, the four Klamath Basin suckers are remarkably similar in all features measured. The 16 haplotypes of ND4L differed by no more than three base pairs from the 'K" haplotype of D. luxatus (Fig. 7). Meristic (Fig. 10) and morphometric (Fig. 14) differences were consistent but slight. For many characters examined, within species variability appeared to blur species-level signal. For example, although species asymptotic gill raker numbers in our ontogenetically adjusted model ranged from 26.1 to
39.9, the r2 was 32.3-72.3 and at any given size one or more species showed overlap (Fig. 8). Also in contrast to expectations from current classification, most of our data tended to support similarity between C. rimiculus and D. luxatus or between C. snyderi and Ch. brevirostris. For example, most C. snyderii and Ch. brevirostris shared ND4L haplotype 'B" .
Despite this overall similarity, we were also able to detect geographic differences in every species. Klamath and
Rogue R. C. rimiculus differed in morphometric and meristic features related to dorsal fin position as well as in fixed differences in ND4L. Both D. luxatus and Ch. brevirostris from Lost River and Upper Klamath subbasins differed in meristic features with higher values in Lost River subbasin. The apparently expatriated Lower Klamath R. Ch. brevirostris tended to be more like fish from the Upper
Klamath subbasin (~igs.21 and 23) . Finally, C. snyderi had morphometric and meristic differences between Upper
Williamson, Sprague and Lost River subbasins. The large- headed Upper Wiliamson C. snyderi also had a unique ND4L haplotype, 'F" .
We can identify 15 nominal hybrids in 326 KLAMGEN specimens with nine being LRS X SNS. Because hybrid morphologies approached both putative parents or was intermediate, mitochondria1 DNA could not identify reciprocal crosses. Assuming reciprocal crosses were equally likely, about 9.2% of our samples showed evidence of outcrossing and since we could not identify SNS X KLS hybrids, the estimate must be low.
There has also been temporal changes in morphology, at least for Ch. brevirostris. Our material of Ch. brevirostris had smaller heads and fewer gill rakers (Fig.
9 and Fig. 15) than lgth century specimens (n=4 and 3, respectively) reported by Miller and Smith (1981). The presence of a common ND4L haplotype, 'B", in Ch. brevirostris and C. snyderi is congruent with Miller and Smith's (1981) suggestion that recent populations of Ch. brevirostris are introgressed with C. snyderi.
Although we agree that older material differs from more recent collections in these characters, we are not convinced that introgression is particularly recent nor that the name Ch. brevirostris is inappropriately applied to recent fish. All of our evidence supports the idea that
Klamath Basin suckers are part of a species complex or syngameon. Syngameons are groups of interbreeding species that maintain their ecological, morphological, genetic and evolutionary integrity in spite of hybridization (Templeton
1989). Hybridization is not inherently 'bad", nor are members of syngameons "bad species". Arnold (1997) notes,
"Rather than viewing hybridization as a problem to be overcome for the process of divergent evolution to proceed, it may be more constructive and instructive to view it as a creative and ongoing process in the evolutionary history of numerous groups of organisms". Species integrity is apparently maintained in syngameons by selection. As
Templeton (1998) notes, "for speciation to occur, it is not necessary for selection to cause the cessation of gene flow, merely to override it."
The great difficulty with Klamath Basin sucker taxonomy is that despite outcrossing, species within the syngameon appear to mate assortatively. Distinct "forms" are recognized by field biologists and show temporal and geographic patterns. For example, all of the large (>380mm
SL) Sprague R. C. snyderi that showed reduced head lengths
(Fig. 23) were caught on 2 or 3 March, 1994 during a
spawning run. Smith (1992) asserted that, "unlike the many examples of salmonids and cottids in lakes, sympatric
fluvial suckers are not known to break into races that home
to different spawning places at different times". However,
tagging results of Klamath Basin D. luxatus and Ch. brevirostris show shoreline lake spawners and river
spawners do not mix (M. Beuttner, U. S. Bureau of
Reclamation, and Rip Shively, U.S.G.S., Biological
Resources Division, personal communication, July, 2000).
Although our samples were insufficient to compare lake and
river spawners (Table 11, we can demonstrate basin or
subbasin differentiation in all species.
Ecological changes in the Klamath Basin can also be
demonstrated. These include hyper-eutrophication of Upper
Klamath Lake, blocking of upstream Sprague R. migration by
Chiloquin Dam, irrigartion diversions, loss of wetland
habitat, and introductions of exotic fishes (Scoppettone
and Vinyard, 1991; Simon and Markle, 1997; Kann and Smith
1999; Martin and Saiki, 1999). There has also been loss of spawning groups. The best known is the loss of the Ch. brevirostris and D. luxatus spawning groups from Harriman
Springs in the northwest corner of Upper Klamath Lake
(Andreasen, 1975). Whether the temporal changes in morphology are due to differential sampling of Harriman
Springs fish in the 18001s, ecophenotypic responses to habitat change, or hybridization is not clear.
Klamath Basin suckers hybridize, but we believe the
four species maintain separate identity. If gene flow approaches lo%, this could only occur with strong
selection. Their high fecundity (up to 235,000 eggs in D.
luxatus, Andreasen 1975) and tetraploid genome may
facilitate such a complex system and studies of nuclear DNA may offer further insight. TABLES
Table 1. Distribution of specimens by species and subbasin for KLAMGEN samples.
Subbasin Nominal Upper I Sprague I Upper I Lost I Lower I Roque- Species Williamson Klamath River Klamath C. snyderi 31 40 1 2 1 C. rimiculus 1 24 30 Ch . 34 104 15 brevirostri s D. luxatus 25 17
Table 2. Glossary for variables used in morphological analyses utilized in study. General terminology follows that of Hubbs and Lagler (1958).
Counts
PCV. Post-Weberian precaudal vertebrae without a definite hemal spine even if a hemal arch was present. CV. Post-Weberian caudal vertebrae with a definite hemal spine including urostyle. INTERIDFP. Number of vertebrae anterior to first dorsal fin pterygiophre including vertebra immediately posterior to point of interdigitation with neural spines. VDO . Number of vertebrae anterior to a vertical from base of first dorsal fin ray including vertebra intersected by the vertical. VAO . Number of vertebrae anterior to a vertical from base of first anal fin ray including vertebra intersected by the vertical. VPO . Number of vertebrae anterior to a vertical from base of first pelvic fin ray including vertebra intersected by the vertical. GILRKRANT. Number of gill rakers on lateral surface of first gill arch. GILRKPOST. Number of gill rakers on medial surface of first gill arch. PGRVAGR. Number of gill rakers on medial surface of first arch anteriad of all gill rakers on the lateral surface of the arch. NASALLAM. Nasal lamellae. PREOPMNPOR. Preoperculomandibular pores. INFORBPOR. Infraorbital pores. IOPAE. Number of infraorbital pores anterior to a vertical from anterior margin of eye. SUPORBPOR. Supraorbital pores. LLSCALES. Lateral line scales. LLPECTPOR. Number of lateralis pores on cleithrum from supratemporal canal to first lateral line scale. DSCALEROW. Diagonal scale rows. SCALEADF. Scales anterior to dorsal fin. SCALABVLL. Scales above lateral line. SCALBELOLL. Scales below lateral line. PAPUPRLIP. Rows of papillae at symphysis of upper lip. PAPLORLIP. Rows of papillae at symphysis of lower lip. SCACADPED. Scales around caudal peduncle
Measurements
FLMM. Fork length (measurements made before preservation) TLMM. Total length (measurements made before preservation) SL. Standard length (measurements made on preserved specimens) FL . Fork length (measurements made on preserved specimens) LAE . Snout length. LPE. Distance from tip of snout to posterior margin of eye. HL . Head length. IW. Interorbital width at narrowest point. WPl . Width of body at pectoral fin bases DP1. Depth of body at anterior margin of pectoral fin bases. Depth of body at dorsal-fin origin. DDO . - LOP2. Distance from tip of snout to pelvic fin origin. LOP1- LOP2. Distance from pectoral fin origin to pelvic fin origin. LOD. Pre-dorsal length. LID. Distance from tip of snout to insertion of dorsal fin. LOA. Pre-anal length. LIA. Distance from tip of snout to insertion of anal fin. LDA. Distance from dorsal fin origin to anal fin origin. LDOC. Distance from dorsal fin origin to middle of caudal fin base. LDIC. Distance from dorsal fin insertion to middle of caudal fin base. CPD. Least caudal peduncle depth. LP1. Length of longest pectoral fin ray. LP2. Length of longest pelvic fin ray. LPEOD. Distance from posterior margin of eye to origin of dorsal fin. LPOA. Distance from pelvic fin origin to anal fin origin. SPMLL. Projected distance from tip of snout to posterior margin of lower lip with mouth closed. LDMM. Distance from symphysis of lower jaw to lateroposterior margin of lower lip lobe. GAPLMM. Distance from symphysis of lower jaw to point where lower lip lobes separate. AIOPAE. Distance from anteriormost infraorbital pore to anterior margin of eye. SAIOP. Distance from tip of snout to anteriormost infraorbital pore. POMMM. Perimeter of mouth. AOMMM. Area of mouth.
Nominal data
LLGAP. Gap between lower lip lobes scored as, Y = present when lower lip lobes do not contact; N = absent when lower lip lobes contact ; T = teratological; A = when a gap is present anteriorly but lips touch posteriorly. LLLRM. Posterior extent of lower lip scored relative to a vertical through ventroposterior corner of maxilla as, A= lip ending anterior, E= even and P= posterior to vertical. VERTFUSION. Presence (Y) or absence (N) of fusion among vertebrae. GRFUSION. Presence (Y) of absence (N) of fusion among gill rakers. LTNASALFLP. Condition of left nasal flap scored as A = absent; D = deformed; C = nare; N = does not cover nare . RTNASALFLP. Condition of right nasal flap scored as A = absent; D = deformed; C = nare; N = does not cover nare . PREOPBRANCH. Branching (Y) or absence (N) of branching in preoperculomandibular canal. INFBRANCH. Branching (Y) or absence (N) of branching in nfraorbital canal. SUPBRANCH. Branching (Y) or absence (N) of branching in supraorbital canal. Table 3. Distribution of mtDNA ND4L haplotypes by species.
Allele N SNS LRS KSS KLS
B 186 95 3 1 87 C 1 1 D 2 2 E 1 1 F 17 G 2 H 1 I 27 3 J 2 1 K 40 33 L 28 M 1 1 N 12 7 2 3 0 1 1 P 1 1 Total 324 114 44 53 113 Figure 1.Map showing parts of Klamath and Rogue basins and subbasin designations used in study.
Figure 2. Relationship between mouth area and mouth perimeter for 33 KLAMGEN specimens.
Figure 3. Lips of Klamath basin suckers, showing posterior extent of lips with lips ending anterior (A), even (B) or posterior (C) to ventroposterior corner of maxillary (arrows). Lower figures illustrating presence of lower lip gaps (D and E) and absence of lower lip gap (F).
Figure 4. Relationships between GAPLMM/EYE and posterior extent of lips.
Figure 5. Relationships between GAPLMM/EYE and presene or absence of lower lip gap.
Figure 6. Lower lips of juvenile suckers, 97-107 mm SL. A and B. C. snyderi, OS 13739. C. and D. Ch. brevirostris, OS 13754.
Figure 7. Phylogeny of ND4L hapolotypes in Klamath and Rogue R. suckers. Numbers on branches indicate number of mutations between haplotypes.
Figure 8. Relationships between gill rakers and size in Klamath and Rogue R. suckers.
Figure 9. Relationship between gill rakers and size in Ch. brevirostris with ontogenetic regression model. Box encloses values reported by Miller and Smith (1981) for nominally "pure" specimens.
Figure 10. First two Principal Componenet (PC) axes for a reduced set of five meristic characters. Coefficients for each character on each axis shown next to axis.
Figure 11. First two Principal Componenet (PC) axes from Figure 10 with species outlined and ND4L haplotypes mapped. A. haplotype 'I", B. haplotype 'K" , and C. haplotype 'B" . Figure 12. Relationship between GAPLMM/E~~ratio and LAE/HD ratio in Klamath and Rogue R. suckers. Figure 13. Data from Figure 12 replotted with ND4L haplotypes mapped. A. haplotype 'B" and B. haplotype 'K".
Figure 14. First two Principal Componenet (PC) axes for a reduced set of 5 residuals of morphometric characters regressed on SL. Coefficients for each character on each axis shown next to axis.
Figure 15. Relationship between the HL/SL ratio and size in Ch. brevirostris I and C. snyderi. Box encloses values reported by Miller and Smith (1981) for nominally "pure" Ch. brevirostris.
Figure 16. Left lateral view of C. rimiculus. A. Klamath R. at J. C. Boyle Reservoir, OS 15909-GI 336 mm S1, female B. Rogue R., OS 15913-Dl 333 mm S1, female.
Figure 17
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