Five Natural Hybrid Combinations in Minnows (Cyprinidae).
by Frank B. Cross and W. L. Minckley.
The hybrid fishes described herein are _Chrosomus erythrogaster_ (Rafinesque) _Notropis cornutus frontalis_ (Aga.s.siz), _C.
erythrogaster_ _Semotilus atromaculatus_ (Mitchill), _Campostoma anomalum plumbeum_ (Girard) _S. atromaculatus_, _Gila nigrescens_ (Girard) _Rhinichthys cataractae_ (Valenciennes), and _Notropis venustus venustus_ (Girard) _Notropis whipplei_ (Girard). Two of the combinations have been reported, without descriptions, in literature (citations below), and Hubbs (1955: Fig. 3) graphically indicated hybridization between the same genera with which this paper is concerned, but did not designate the species involved.
All specimens of _C. erythrogaster_ _N. c. frontalis_, _C.
erythrogaster_ _S. atromaculatus_, _C. a. plumbeum_ _S.
atromaculatus_, and _N. v. venustus_ _N. whipplei_ were taken in a period of severe drought in Kansas and Arkansas. All were from small, spring-fed streams that support large populations of fishes. That the drought of 1953-1956 had p.r.o.nounced effects on stream habitats in Kansas has been doc.u.mented by Minckley and Cross (1959). Satisfactory sites for sp.a.w.ning may have been few, but an abundance of adult fishes persisted from earlier, wet years. Unusual crowding of sp.a.w.ning fishes would increase the opportunity for fertilization of the eggs of one species by sperm from another species. We think that the hybrids reported here (excepting _G. nigrescens_ _R. cataractae_) are explainable on the basis of crowding; we have no information about stream-conditions where the last-named hybrid was found. Generally, hybridization of fishes seems most common in areas that have been subject to radical climatic change in the past 20,000 or fewer years (Hubbs, 1955:18-19), and in streams that have been altered recently by the activities of man (Hubbs and Strawn, 1956:342, and others). Streams from which we report hybrids probably were affected by overgrazing of their watersheds; overgrazing was unusually severe in the drought.
Most of the hybrids were recognized as unusual at the time of capture, and were saved as part of numerically selective samples from the streams (rather than being discovered in the laboratory, in random samples).
Our measurements were made by methods defined by Hubbs and Lagler (1958); values are expressed as thousandths of the larger dimension.
=_Chrosomus erythrogaster_ _Notropis cornutus frontalis_=: KU 3872 (26.7 mm. in standard length) and KU 4170 (46.6 mm.) from Deep Creek, Riley Co., Kansas, Sec. 23, T. 11S, R. 7E, Dec. 14, 1957, and Apr. 26, 1958, respectively; and KU 4185 (39.3 mm.) from Bluff Creek, Pottawatomie Co., Kansas, Sec. 15, T. 6S, R. 8E, June 29, 1958. Compared in Table 1 with five specimens of _C. erythrogaster_, KU 3914 (39.3 to 47.3 mm., mean 43.0 mm.) from the same locality and of the same date as KU 3872 (above); and with five specimens of _N. c. frontalis_, KU 4184 (41.0 to 46.5 mm., mean 42.5 mm.) from the same locality and of the same date as KU 4185 (above). This cross has previously been recorded by Trautman (1957:326, 355) and by Minckley (1959:431).
The head-lengths of the hybrids are greater than in specimens of like size of _C. erythrogaster_ or _N. c. frontalis_ (Table 1). Hubbs and Miller (1943:373-374) reported that hybrids of _Gila orcutti_ _Siphateles mohavensis_ have larger, more robust heads than either of the parental species, perhaps because of heterosis. The enlarged heads in hybrids of _C. erythrogaster_ and _N. c. frontalis_ result primarily from elongation of the pos...o...b..tal region, with lesser elongation of the snout and orbit. The enlarged head affects measurements obtained for other structures that are parts of the head (and expressed as proportions of standard length or head-length), causing a tendency toward _N. c. frontalis_ when the head-part is divided by standard length, and greater intermediacy or a tendency toward _C. erythrogaster_ when the head-part is divided by head-length. In characters in which the parental species differ most (size of eye, length of upper jaw, and width of gape), the hybrids are intermediate between the parental species, regardless of whether the measurements are expressed as proportions of head-length or standard length; however, tendencies toward one or the other of the parental species (dependent on the divisor) can also been seen in these characters. Some experimentally propagated hybrids show highly variable, and sometimes extreme characters, rather than intermediacy of meristic and proportional characters (Hubbs, 1956).
TABLE 1. COMPARISONS OF THREE SPECIMENS OF CHROSOMUS ERYTHROGASTER NOTROPIS CORNUTUS FRONTALIS WITH SPECIMENS OF THE PARENTAL SPECIES (MEANS ARE ABOVE, RANGES IN PARENTHESES BELOW)
=====================+=============+=============+=========+==============_Chrosomus erythrogaster_KU 4170 and 4185KU 3872_Notropis__c. frontalis_ ---------------------+-------------+-------------+---------+-------------- Standard lengths43.043.026.742.5(39.3-47.3)(39.3-46.6)...(41.0-46.5)Head-length /253282307276 Standard length(246-262)(280-283)...(273-283)Orbital length /067075101083 Standard length(063-071)(071-079)...(080-086)Orbital length /263266329300 Head-length(252-272)(250-282)...(291-310)Snout-length /069073071068 Standard length(068-071)(071-075)...(066-071)Snout-length /272260232245 Head-length(262-280)(255-265)...(233-260)Interorbital width /069074079068 Standard length(065-071)(069-079)...(067-069)Interorbital width /272263256245 Head-length(262-286)(245-280)...(241-250)Gape-width /056065064065 Standard length(051-059)(059-071)...(062-066)Gape-width /222230207233 Head-length(204-241)(209-250)...(224-239)Upper jaw-length /057082112083 Standard length(051-061)(076-088)...(080-086)Upper jaw-length /223292268301 Head-length(206-237)(273-311)...(284-315)Pos...o...b..tal length /113130124123 Standard length(108-120)(129-130)...(121-125)Pos...o...b..tal length /444460402446 Head-length(432-456)(455-464)...(431-457)Length of depresseddorsal fin /224250255237 Standard length(217-232)(247-252)...(233-243)Length of depresseddorsal fin /885886829858 Head-length(869-892)(871-900)...(836-890)Number scales inlateral line71.753.052(?)38.8(68-76)(53.0)...(38-39)Pharyngeal teeth0,5-5,01,5-4,11,5-4,22,4-4,2((?)-4,1)a.n.a.l rays888usually 9Vertebrae37-4039...38-39 ---------------------+-------------+-------------+---------+--------------
In pigmentation, all three of the hybrids are intermediate between the parental species. The mid-lateral band (which is dark and discrete in _C. erythrogaster_, but faint, broad, and diffuse in _N. c. frontalis_) is broader and fainter in the hybrids than in _Chrosomus_, but is better developed than in _N. c. frontalis_. The dorsolateral dark band of _C.
erythrogaster_ is present in the hybrids, but is less distinct than in that species, and less distinct than the mid-lateral band of the hybrids themselves. The dorsolateral band is not present in _N. c. frontalis_.
The color of the peritoneum in the hybrids is the glossy, jet-black of _C. erythrogaster_ in two specimens, and the dusky-black of _N. c.
frontalis_ in one.
_Chrosomus_ and _Notropis_ differ greatly in the length and convolution of the intestine. _Chrosomus_ has a long, coiled gut, which is crossed by the mid-ventral line eight or nine times; in _N. c. frontalis_, the intestine forms a flat, S-shaped loop that does not cross the mid-ventral line. In the two largest hybrids (KU 4170 and 4185), the gut is intermediate, crossing the mid-ventral line four times. In the smaller hybrid (KU 3872) the gut crosses the mid-ventral line twice but the configuration of the anterior loops indicates that the same intestinal convolutions that were found in the larger specimens would have developed in KU 3872 as the gut elongated with increase in size of the fish.
Both Deep and Bluff creeks are clear, gravel-bottomed streams draining parts of the Flint Hills Area of Kansas. A description of Flint Hills streams and lists of fishes occurring in them have been published by Minckley (1956 and 1959), and by Minckley and Cross (1959).
=_Chrosomus erythrogaster_ _Semotilus atromaculatus_=: KU 2947 (28.0 mm. in standard length) from Mill Creek, Wabaunsee Co., Kansas, Sec. 30, T. 12S, R. 9E, Mar. 22, 1953. Compared in Table 2 with five specimens of _C. erythrogaster_, KU 2836 (27.2 to 31.0 mm., mean 28.5) from the same locality and of the same date as KU 2947 (above); and with five specimens of _S. atromaculatus_, KU 1954, 2499, 2703, and 2838 (25.5 to 31.1 mm., mean 28.9 mm.) from streams in the same area.
This hybrid is intermediate between the two species in number of scales and pharyngeal teeth, and has a composite of the pigmentation found in the parental fishes (Table 2). For diagnostic purposes, greater importance is attached to the characters mentioned above than to proportional measurements, which are subject to considerable error because of the small size of the specimens. The few measurements that were taken indicate that this hybrid, like _C. erythrogaster_ _N. c.
frontalis_, has a larger head than do specimens of like size of either parental species. The enlarged head affects measurements obtained for other structures that are parts of the head; only the length of the upper jaw, which is greatly different in the parental species, is actually intermediate in KU 2947.
Mill Creek is a clear stream, similar to Deep and Bluff creeks but somewhat larger. Mill Creek had an exceptionally large population of fishes at the time the hybrid was found, but _Chrosomus_ and _Semotilus_ were neither unusually common nor rare.
Two other crosses, both of which have been described in the literature, also have been found in Mill Creek. These are _N. c. frontalis_ _S.
atromaculatus_, and _N. c. frontalis_ _Notropis rubellus_ (Aga.s.siz).
TABLE 2. COMPARISON OF ONE SPECIMEN OF CHROSOMUS ERYTHROGASTER SEMOTILUS ATROMACULATUS WITH SPECIMENS OF THE PARENTAL SPECIES (MEANS ARE ABOVE, RANGES IN PARENTHESES BELOW)
========================+==============+================+=================_Chrosomus erythrogaster_KU 2947_Semotilus__atromaculatus_ ------------------------+--------------+----------------+----------------- Dark lateral bandintenseintenseintenseLight dorsolateral bandwell-definedpoorlyabsentdevelopedDark dorsolateral bandintensepoorlyabsentdevelopedColor of peritoneumblackblacksilveryLength of gutlong withshort, with ashort, with atransversesingle forwardsingle forwardcoilslooploopPharyngeal teeth0,5-5,01,5-5,2usually 2,5-4,2Number scales inlateral lineusually 70about 67usually feweror more,slightlythan 65, notembeddedembeddedembeddedBarbelsabsentabsentusually presentVertebrae37-403942-43Head-length /272310300 Standard length(266-277)(292-308)Upper jaw-length /071097110 Standard length(069-074)(104-114)Upper jaw-length /263310366 Head-length(254-273)(356-382)Interorbital width /103114116 Standard length(101-106)(114-118)Interorbital width /381372388 Head-length(372-400)(380-400)Orbital length /081083078 Standard length(075-085)(076-084)Orbital length /296267261 Head-length(271-313)(255-273) ------------------------+--------------+----------------+-----------------
=_Campostoma anomalum plumbeum_ _Semotilus atromaculatus_=: KU 4013 (three males, 86.0 to 96.0 mm. in standard length, mean 89.5 mm.) from Timber Creek, Scott Co., Kansas, Sec. 2, T. 16S, R. 33W, June 19, 1958. Compared in Table 3 with five specimens of _C. a. plumbeum_, KU 4034 (85.7 to 93.1 mm., mean 90.2 mm.) from the Smoky Hill River, Wallace Co., Kansas, Sec. 26, T. 13S, R. 39W, June 20, 1958; and with five specimens of _S. atromaculatus_, KU 4012 and 4047 (85.0 to 97.5 mm., mean 91.7 mm.) from the same locality and of the same date as KU 4013 (above), and Sappa Creek, Decatur Co., Kansas, Sec. 29, T. 2S, R.
28W, June 23, 1958, respectively. This hybrid combination has previously been recorded by Johnson (1945).
TABLE 3. COMPARISONS OF THREE SPECIMENS OF CAMPOSTOMA ANOMALUM PLUMBEUM SEMOTILUS ATROMACULATUS WITH SPECIMENS OF THE PARENTAL SPECIES (MEANS ARE ABOVE, RANGES IN PARENTHESES BELOW)
=====================+=================+===============+=================_Campostoma a._KU 4013_Semotilus__plumbeum_(three spec.)_atromaculatus_ ---------------------+-----------------+---------------+----------------- Standard lengths90.289.591.7(85.7-93.1)(85.7-96.2)(85.0-97.5)Predorsal length /511533557 Standard length(505-517)(523-542)(547-564)Head-length /251276289 Standard length(244-258)(273-278)(280-299)Snout-length /090088085 Standard length(086-096)(087-091)(082-087)Orbital length /044048049 Standard length(043-045)(047-049)(048-050)Interorbital width /075094110 Standard length(073-078)(091-099)(104-113)Distance from tip ofmandible to tip ofmaxillary /057076098 Standard length(053-063)(072-078)(095-104)Gill rakers30179 (1st arch)(29-31)(16-18)(8-10)Number scales in545456 lateral line(53-55)(54-55)(52-64)Predorsal scale-rows252735(23-27)(27-28)(34-36)a.n.a.l rays77.38(6-7)(7-8)8Vertebrae4042-44[A]42-43 ---------------------+-----------------+---------------+-----------------
[A] Three deformed vertebrae in one specimen with 44; other two specimens have 42 vertebrae.
The hybrids seem uniformly intermediate between the parental species.
Application of the hybrid index to the characters listed in Table 3 results in a value of 55.7 when _C. a. plumbeum_ is a.s.signed the value 0.
The pharyngeal arches of the hybrids are peculiarly deformed. Expressed in terms of the one-or two-rowed arrangement common to all North American cyprinids, tooth-counts of 0,5-4,1; 1,3(?)-4,0; and 2,5-4,1 best fit the three fish. However, one arch bears only three teeth, all deformed and badly aligned, plus a pit that presumably represents a lost fourth tooth. At the other extreme, one arch bears eight teeth, some of which are attached to the arch between and behind others that are countable as part of the basic main row. Supernumerary teeth and other deformities may have resulted from abnormalities in the replacement process. In some cases, replacement teeth probably failed to develop; in others, replacement teeth seemingly developed, but attached to the arch in abnormal positions, with or without loss of previous teeth, causing irregularity in alignment. Hubbs (1951) described an irregular (seemingly three-rowed) alignment in a fish that Hay (1888:249) reported from western Kansas as _Squalius elongatus_. However, Hubbs considered the specimen to be an aberrant example of _S. atromaculatus_, and the characteristics that he lists for it do not correspond closely with those of the hybrid specimens that we have. Evans and Deubler (1955:32) found three rows of teeth in two of 150 specimens of _Semotilus_, and attributed the abnormality to failure of old teeth to fall out after formation of new teeth. The teeth of _Campostoma_ usually number 0,4-4,0, and those of _Semotilus_ 2,5-4,2. The pharyngeal arches are much smaller in _Campostoma_ than in _Semotilus_.
The peritoneum is mottled dark and silvery in the hybrids; it has a composite of the coloration in the parental species rather than a blended shade. The intestine has two diagonal loops crossing the ventral part of the body cavity, and the hindgut lies high in the cavity, along the left side of the air bladder. In _Campostoma_, the long gut is transversely coiled around the air bladder, whereas in _Semotilus_ the gut forms a longitudinal, flattened, S-shaped loop, ventral to the air bladder.
In the hybrids, the mouth is slightly oblique and nearly terminal. The lower lip is thick and fleshy, but has only a suggestion of the projecting mandibular shelf that is unique in _Campostoma_. The upper lip is uniform in width, not medially expanded as in _S. atromaculatus_.
One of the hybrids lacks barbels, one has a _Semotilus_-like barbel on the right side only, and one has a vestigial barbel on the right side and an anomalous barbel that is nearly terminal on the left upper lip.
In coloration, the hybrids lack the spot in the anterior base of the dorsal fin that is characteristic of _Semotilus_, but each has a poorly-developed dark lateral band, and a weak basicaudal spot. This band and spot are usually prominently developed in _S. atromaculatus_ and usually are absent in adults of _C. a. plumbeum_.
In the position and obliquity of the mouth, basic color pattern (diffuse lateral band and basicaudal spot), and the presence in one specimen of a nearly terminal, barbel-like structure, the hybrids somewhat resemble _Hybopsis biguttata_ (Kirtland), which occurs rarely in the Kansas River Basin. These partial similarities are coincidental, because other characters of the hybrids make relationship with _H. biguttata_ implausible. The high number of gill rakers (Table 3) and the length and position of the gut indicate strongly that the three specimens are hybrids with _C. anomalum_ as one parent; the pharyngeal arches, though deformed, indicate that the other parental species has two rows of teeth, with five teeth in the main row. Only _S. atromaculatus_, among species in the Kansas River Basin, usually has such a dental formula, and other characters of our three specimens fit expectations in a hybrid between that species and _C. a. plumbeum_.
Timber Creek, where the three hybrids were collected, is a small, spring-fed, sandy-bottomed tributary to Scott County State Lake in the extreme southwestern part of the Kansas River Basin. The stream was less than 10 feet wide and six inches deep, except in three pools near road crossings. The hybrids were found in two of these pools, along with numerous _S. atromaculatus_ and one adult _C. a. plumbeum_.
Another specimen of _C. a. plumbeum_ _S. atromaculatus_ (KU 4841, 39.3 mm. in standard length) was taken in the North Platte River at Lisco, Garden County, Nebraska, on September 11, 1959. That specimen has 7 a.n.a.l rays and 52 scales in the lateral line; otherwise, it is similar to the three hybrids described above.
=_Gila nigrescens_ _Rhinichthys cataractae_=: KU 4253 (a male, 60.6 mm. in standard length), from New Mexico, Bernalillo County, Rio Grande 12 mi. S Bernalillo on U. S. Highway 85 (Corraleo Bridge). Compared in Table 4 with six specimens of _G. nigrescens_: KU 4251, 4254, and 4262 (63.1-72.4 mm. in standard length, mean 66.4 mm.); and with five specimens of _R. cataractae_: KU 4248, 4258, and 4264 (55.6-65.0 mm.
standard length, mean 59.5 mm.). Comparative material was taken at the same locality as KU 4253 and at nearby localities in the Rio Grande.
The hybrid is intermediate in almost all of the features in which the parental species differ from each other. For six of the characters included in Table 4, the hybrid index is 49.7 per cent, when _Gila_ is a.s.signed the value 0 (height of dorsal fin and numbers of fin rays and teeth excluded). There is no enlargement of the head in KU 4253, such as was found in _Gila orcutti_ _Siphateles mohavensis_ (Hubbs and Miller, 1943:373), _Chrosomus erythrogaster_ _Notropis cornutus frontalis_, and _C. erythrogaster_ _Semotilus atromaculatus_. The height of the dorsal fin, which Hubbs and Miller (_loc. cit._) found to be extreme in _G. orcutti_ _S. mohavensis_, exceeds the average for the parental species in _G. nigrescens_ _R. cataractae_ also; but, dorsal fins as high as that of the hybrid were found in some individuals of both parental species. In _R. cataractae_, all fins are more rounded and more expansive than in _G. nigrescens_, and fins other than the dorsal have an intermediate size in the hybrid. This intermediacy has doubtful significance, because fin-size in _Rhinichthys_ varies greatly with body-size, s.e.x, and probably with the state of s.e.xual development.
_Rhinichthys_ matures at smaller size than _Gila_, and never becomes so large as that species.
_Gila nigrescens_ and _R. cataractae_ differ strikingly in features involving the snout and mouth, and these differences provide the most conclusive evidence that KU 4253 is a hybrid of these species. The projecting, fleshy snout of _R. cataractae_ is bridged to the ventral mouth by a frenum that is approximately 3 mm. wide in specimens 60 mm.
in standard length. In _Gila_, the snout does not project beyond the mouth, which is oblique, lacks a frenum, and is larger than in _Rhinichthys_. The snout of the hybrid projects less than in _R.
cataractae_ and is bridged to the upper lip by a frenum 1.7 mm. wide.
The mouth of the hybrid is intermediate in size, obliquity, and thickness of the lips. _Rhinichthys_ has barbels, _Gila_ lacks them, and the hybrid has one vestigial barbel, on the right side. The lower surface of the head of _Rhinichthys_ is broad and flattened, with p.r.o.nounced rugosity on the gular area and isthmus. In _Gila_ the underside of the head is convex, with comparatively smooth membranes; the hybrid is intermediate, but tends toward _Gila_.
TABLE 4. COMPARISONS OF ONE SPECIMEN OF GILA NIGRESCENS RHINICHTHYS CATARACTAE WITH SPECIMENS OF THE PARENTAL SPECIES (MEANS ARE ABOVE, RANGES IN PARENTHESES BELOW)
======================+==============+=================+=================_Gila__Rhinichthys__nigrescens_KU 4253_cataractae_ ----------------------+--------------+-----------------+----------------- Standard lengths66.460.659.5(63.1-72.4)(55.6-65.0)Head-length /282281281 Standard length(277-290)(273-293)Orbital length /063054044 Standard length(063-065)(041-047)Snout-length /083092106 Standard length(081-085)(099-113)Dorsal fin-height /225234221 Standard length(212-238)(206-234)Pos...o...b..tal length /140135131 Standard length(134-142)(127-136)Distance from tip ofmandible to tip ofmaxillary /081076066 Standard length(079-085)(064-069)Length ofinfral.a.b.i.al groove /060045036 Standard length(058-064)(034-038)Upper jawprotractilenon-protractilenon-protractileNumber scales inlateral line606365(58-63)(63-67)a.n.a.l fin-rays877(7-8)(7)Pelvic fin-rays988(9)(8-9)Pectoral fin-rays1616-1513(16-18)(13-14)Pharyngeal teeth2,5-4,22,5-4,22,4-4,2 ----------------------+--------------+-----------------+-----------------
TABLE 5. COMPARISONS OF ONE SPECIMEN OF NOTROPIS V. VENUSTUS NOTROPIS WHIPPLEI WITH SPECIMENS OF THE PARENTAL SPECIES, AND WITH N. LUTRENSIS N. V. VENUSTUS. MEASUREMENTS (LENGTHS AND DEPTHS) ARE EXPRESSED AS THOUSANDTHS OF STANDARD LENGTH (MEANS ABOVE, RANGES IN PARENTHESES BELOW)
Column headings:
A: _Notropis whipplei_ B: KU 3516 C: _Notropis venustus_, KU 3510 D: _Notropis venustus_, from Gibbs (1957a) E: _Notropis lutrensis_ _N. venustus_
=================+=============+=========+=============+=========+=============ABCDE -----------------+-------------+---------+-------------+---------+------------- Standard length50.647.847.344.7(45.0-54.0)(44.5-49.6)(43.3-47.3)Predorsal length525523534523532(513-535)(519-547)(528-538)Dorsal origin tocaudal base497508497496508(493-502)(478-504)(502-514)Prepelvic length505492505499(498-518)(500-510)(486-517)Head-length257255261260263(250-262)(256-267)(261-267)Caudalpeduncle-length217221224224(211-220)(213-230)(214-231)Caudalpeduncle-depth110119127125126(106-116)(124-133)(122-131)Head-depth170182186190(167-173)(182-190)(189-192)Snout-length079079080081(076-083)(072-083)(078-082)Eye-diameter069069070073[A]070(063-078)(066-072)(068-074)Pos...o...b..tallength, head112115116117(108-115)(112-120)(115-120)Upper jaw,length078077081079077(076-081)(076-082)(076-081)Body depth239253278274282(233-248)(261-288)(275-294)Lateral-linescales36-373636-3836.5(34-39)Scales abovelateral-line13141515(13-16)a.n.a.l fin-rays9988(7-8)Pectoralfin-rays1414-141514.2(14-15)(14-16)(12-17)Caudal spotAbsentPresentPresentPresentPresentVertebrae37-383837-----------------+-------------+---------+-------------+---------+-------------
[A] Orbital diameter.