Cyprinodon rubrofluviatilis

Red River pupfish

Type Locality

Brazos River, between Seymour and Authon, Texas; and the Red River, Tulip and Clarenden, Texas (Fowler 1916).

Etymology/Derivation of Scientific Name

Cyprinodon bovinus rubrofluviatilis named for the Red River, of the most northern inland eastern region at which a member of the genus Cyprinodon has been found (Fowler 1916).

Synonymy

Cyprinodon bovinus rubrofluviatilis Fowler 1916:430-432.

Characters

Maximum size: Up to 58 mm TL (Page and Burr 1991).

Coloration: Juveniles, females, non-breeding males with color pattern primarily consisting of a lateral and dorso lateral series of brownish irregularly shaped blotches; iris of eye black or silvery and a black with black teardrop marking variably distinct below the eye (Echelle 1973). In females, lateral blotches more attenuated ventrally, roughly triangular; in males, lateral blotches more rectangular; females with melanistic spot at base of dorsal fin that is lacking in males larger than 20-25 mm TL; males with faint remnant of the caudal band that characterizes breeding males (Echelle 1973). Breeding males typically have blackened iris and suborbital teardrop marking; bright blue iridescence in upper body, most intense in nape region; light to bright yellow in face, pectorals (may have black around edges), pelvics, and lower half of body anterior to caudal peduncle; dorsal and anal fins gray to black with hyaline to white borders posteriorly; caudal fin dusky gray to whitish, bordered posteriorly with an intense black band; colors are less intense during periods of relative inactivity and more intense during sustained periods of courtship and/or antagonistic activity; during sustained periods of courtship/antagonistic behavior, the area between the caudal band and the caudal base appears chalky-white, and usually 4 or 5 variably distinct vertical bars, grayish-blue to maroon with bluish cast, are visible on the sides of the body (Echelle 1973). Eyes of breeding males almost always black except during extreme fright when they become silvery; females and nonbreeding males with black eyes tend to be more aggressive than those with silver eyes (Echelle 1973).

Counts: Scales in lateral series 24-26; 9 dorsal fin rays; 8-9 anal rays (Miller and Robison 2004).

Mouth position: Upturned (Page and Burr 1991). Lower jaw slightly protruding in front, oblique to somewhat vertical, shallow, and rami not elevated inside mouth (Fowler 1916).

Body shape: Caudal peduncle depth less than distance from snout to back of eye; in adults, greatest body depth contained less than two and one-half times in standard length; distance from origin of dorsal fin to end of hypural plate less than distance from origin of dorsal to anterior nostril (Hubbs et al. 1991). Body well compressed, deepest at dorsal origin, predorsal with median trenchant keel and well arched before dorsal fin; caudal peduncle compressed, its least depth one and one-fifth in its length; head compressed moderately, upper profile more inclined than lower, and lower sides not especially converging below; snout short, wide, and length about two-thirds its width; eye moderate, high, center about first two-fifths in head (Fowler 1916). Small mouth (Page and Burr 1991).

External morphology: Abdomen naked anterior to pelvic fins (Hubbs et al. 1991). Lateral line scales large; caudal fin square; dorsal, anal and pelvic fins relatively small (Miller and Robison 2004).

Internal morphology: Teeth compressed and with three cusps (Fowler 1916; Hubbs et al. 1991). Renfro and Hill (1972) discussed cytological adaptation in the gills of Cyprinodon rubrofluviatilis.

Distribution (Native and Introduced)

U.S. distribution: Red and Brazos Rivers, Oklahoma and Texas (Minckley et al. 1991). Introduced in the South Canadian River (Arkansas River System), Oklahoma (Pigg 1983; Pigg et al. 1995), and in the Cimarron River drainage, Oklahoma where it has become established (McNeely et al. 2004). Pigg et al. (1997) reported collection of specimen from the Salt Fork of the Arkansas River in Oklahoma.

Texas distribution: Species occurs naturally in the upper Red and Brazos basins. Introduced populations also exist in the Canadian and Colorado basins (Echelle et al. 1977; Minckley 1980; Hubbs et al. 1991; Page and Burr 1991).

Abundance/Conservation status (Federal, State, NGO)

Secure and widespread, although groundwater use increasing (Minckley et al. 1991). One of the seven most abundant fish species collected in the upper Brazos River basin (Ostrand and Wilde 2002). Anderson et al. (1983) reported collection of three specimens from a site above Possum Kingdom Reservoir (Brazos River, Texas) which was sampled each month for a year; no individuals were collected at sites downstream from the reservoir. Miller and Robison (2004) stated that species is common in the sandy-bottomed rivers and streams of southwestern Oklahoma. Taylor et al. (1993) sampled 48 sites in the upper Red River drainage (southwestern Oklahoma) from March-May 1989 and reported relative abundance of 0.01 for Cyprinodon rubrofluviatilis with 362 individuals collected from 19 sites.

Habitat Associations

Macrohabitat: Headwater streams of xeric grasslands (Echelle et al. 1972b; Minckley 1980).

Mesohabitat: River edges, channels, backwaters, over sand bottoms; euryhaline and eurythermal (Minckley et al. 1991). Found in waters where maximum depth is only a few cm; water clear except in flood, and soft-bottomed (Minckley 1980). Ostrand and Wilde (2001) reported mean critical thermal maxima of 38.8 ± 0.8°C at an acclimation temperature of 25°C; at an acclimation temperature of 30°C, mean = 40.3 ± 0.5°C; salinity tolerance (LC50 = 46 ± 0.03‰); species tolerated low dissolved oxygen concentration (mean = 0.95 ± 0.07 mg/L). Occurs in shallow waters where temperatures range from ˉ1 to 39°C (Echelle et al. 1972b). Species has high salinity tolerance (Hill and Holland 1971; Minckley 1980; Higgins and Wilde 2005); restricted to the more saline tributaries of the Red River (Stevenson et al. 1974); present in waters having salinity of 150‰ (Echelle et al. 1972b); present in pools of the Brazos River, Texas, with salinities as high as 110‰ (Ostrand and Wilde 2004). Species tolerant of very high concentrations of dissolved oxygen, up to 20.0 ppm (Hill et al. 1978).

Biology

Spawning season: Late February through early November at temperatures of 13-34°C, with shift from primarily afternoon spawning in winter to primarily morning spawning in warmer months (Echelle 1970; Echelle et al.1972a; Echelle 1973); maximum spawning frequencies observed at midmorning hours in July and August.

Spawning habitat: Occurs in territories maintained by individual males on the bottom of the stream; territories typically in shallowest waters up to 50 cm over sandy shoals and in small coves with little or no current; in areas of moderate current territories were situated near the edge of water and were elongated in the direction of water flow; in water deeper than 1 m, males defended areas over large boulders and clusters of woody debris; all territories varied from two or three times the length of the resident male to approximately 4 m² in area (Echelle 1973).

Spawning behavior: Echelle (1970, 1973) described spawning behavior: males displayed “looping”, “zigzagging”, “headflicking”, “herding” and “steering” preliminary courtship behaviors. While in spawning territory, female usually tilts head downward and nips substrate which stimulates male to swing his body laterally toward her in “sidling” movement, while his body is moved into S-shape and his anal fin is extended toward female in a “wrapping” attempt. Male “clasps” female, his anal fin wrapped around the venter of female and she is pressed against the substrate. Pair vibrates rapidly during clasping; female gives final convulsive jerk as single egg is extruded and male emits sperm; contact is broken; male may attempt “sidling” again. Some aspects of the process may be repeated or female may flee directly from the territory (Echelle 1970; Echelle 1973). Breeding territoriality seemed to function primarily as protection for eggs and to provide adequate space for resident males to court females with minimal interference from other males (Echelle 1970, 1973).

Fecundity: Eggs successfully incubated at temperatures between 14.0 and 36.4°C (Echelle et al. 1972b). Echelle et al. (1973) reported maximum egg diameters of 1.0-1.5 mm; all eggs above 0.8 mm in diameter were pale, transparent yellow in appearance and were in final stages of maturation; in aquaria, individuals maintained at test temperature of 15°C had greater mean egg diameters and gonosomatic indexes than those at 30°C.

Age at maturation:  Echelle et al. (1972a, 1973) stated that this species spawns at small body sizes of 15-20 mm TL.

Migration: Echelle (1970) reported a general upstream migration in one area, in early spring, and only “local movement” of the population at other times of the year; these movements may serve to disperse breeding males, increase male-female encounters, and increase efficient utilization of food resources.

Growth and Population structure: Largest population sizes occur in areas inhabited by few other species, largely due to the great tolerance C. rubrofluviatilis has to physical and environmental extremes (Minckley 1980).

Longevity:

Food habits: Feeds on midge and other insect larvae (Miller and Robison 2004). Intensely active, bottom-feeding omnivore (Echelle 1973); but some feeding occurs at surface and in mid-water (Echelle 1970; Echelle et al. 1972). Individuals frequently displayed bottom-oriented “nipping” and “digging” movements (up to 60-70 acts counted per minute during peak feeding; Echelle et al. 1972a), involving a head-down tilting of the body followed by a return to horizontal position; “plowing” and associated feeding behaviors also observed; feeding occurred at temperatures ranging from 4-40°C; feeding rates varied with temperature, perhaps based on metabolic demand: on warmer summer days, feeding increased from dawn until mid-afternoon, remaining high until just before nightfall; breeding males fed less than breeding females due to time required for courtship and territorial defense; when schooling fish stopped to feed, aggression increased and feeding territories were defended with “circling”, “charging”, “arching” and “tailbeating” behaviors (Echelle 1970; Echelle 1973). Echelle et al. (1973) reported that individuals maintained at 15°C in aquaria were relatively inactive and nonaggressive, while those at 30°C maintained a constant state of feeding activity and continuously competed for feeding sites in an aggressive manner, even though there was an abundance of food; Echelle (1973) reported similar behavior at high temperatures. Minckley and Arnold (1969) noted “pit-digging” behavior by this species in nature, achieved by “in-place-swimming” (Echelle, pers. comm.) and by “plowing”; in the laboratory, individuals built many small (5 cm) pits in aquaria, but did not excavate in algae-filled outdoor pools. During in-place-swimming, the individual actively undulates belly and fins against the substrate; plowing involves sediment being pushed with the head and body (Minckley and Arnold 1969); these behavioral patterns function to excavate large amounts of substrate for the apparent purpose of exposing buried food items (Echelle et al. 1972a).  Rabe et al. (1973) presented data that suggested neither green nor bluegreen algae was digested by this species.

Phylogeny and morphologically similar fishes

Cyprinodon rubrofluviatilis derived from an ancestor similar to the sheepshead minnow (C. variegatus) that invaded the Rio Grande region and moved to adjacent exo and endorheic basins of High Plains and Chihuahuan deserts to give rise to a number of species (Miller and Echelle 1975; Minckley 1980). May be most closely related to the Pecos pupfish (C. pecosensis) of adjacent Pecos River system (Echelle and Echelle 1978; Minckley 1980).

The Red River and Brazos River populations of C. rubrofluviatilis may be genetically distinct at the species level (Hubbs et al. 1991; Ashbaugh et al. 1994).

The plains killifish (Fundulus zebrinus) occurs sympatrically with Cyprinodon rubrofluviatilis in the Red and Brazos Rivers and is closely associated, ecologically and phylogenetically, with the Red River pupfish (Echelle 1970; Echelle et al. 1972a).

Host Records

Commercial or Environmental Importance

Juvenile Cyprinodon rubrofluviatilis may be preyed upon by the red shiner (Cyprinella lutrensis; Gido et al. 1999). Species used successfully in experimental stream units and have produced larvae in the streams (Matthews et al. 2006). Species utilized in hybridization experiments (Cokendolpher 1980).

[Additional literature noting collection of this species from Texas locations includes, but is not limited to the following: Hubbs (1957); Anderson et al. (1983); Echelle et al. (2005).]

References

Anderson, K.A., T.L. Beitinger, and E.G. Zimmerman. 1983. Forage fish assemblages in the Brazos River upstream and downstream from Possum Kingdom Reservoir, Texas. Journal of Freshwater Ecology 2(1):81-88.

Ashbaugh, N.A., A.A. Echelle, and A.F. Echelle. 1994. Genic diversity in Red River pupfish Cyprinodon rubrofluviatilis (Atheriniformes: Cyprinodontidae) and its implications for the conservation genetics of the species.
Journal of Fish Biology 45(2):291–302.

Cokendolpher, J.C. 1980. Hybridization experiments with the genus Cyprinodon (Teleostei: Cyprinodontidae). Copeia 1980(1):173-176.

Echelle, A.A. 1970. Behavior and ecology of the Red River pupfish, Cyprinodon rubrofluviatilis. Ph.D. Dissertation, University of Oklahoma, Norman. 125 pp.

Echelle, A.A. 1973. Behavior of pupfish, Cyprinodon rubrofluviatilis. Copeia(1):68-76.

Echelle, A.A., and A.F. Echelle. 1978. The Pecos River pupfish, Cyprinodon pecosensis n. sp. (Cyprinodontidae), with comments on its evolutionary origin. Copeia 1978(4):569-582.

Echelle, A.A., A.F. Echelle, and F.B. Cross. 1977. First records of Cyprinodon rubrofluviatilis (Cyprinodontidae) from the Colorado and Arkansas River systems, Texas. The Southwestern Naturalist 22(1):142-143.

Echelle, A.A., A.F. Echelle, and L.G. Hill. 1972a. Interspecific interactions and limiting factors of abundance and distribution in the Red River pupfish, Cyprinodon rubrofluviatilis. American Midland Naturalist 88(1):109-130.

Echelle, A. A., C. Hubbs, and A.F. Echelle. 1972b. Developmental rates and tolerances of the Red River pupfish, Cyprinodon rubrofluviatilis. The Southwestern Naturalist 17(1):55-60.

Echelle, A.A., E.W. Carson, A.F. Echelle, R.A. Van Den Bussche, T.E. Dowling, and A. Meyer. 2005. Historical biogeography of the new-world pupfish genus Cyprinodon (Teleostei: Cyprinodontidae). Copeia 2005(2):320-339.

Echelle, A.A., S. Wilson, and L.G. Hill. 1973. The effects of four temperature-daylength combinations on ovogenesis in the Red River pupfish, Cyprinodon rubrofluviatilis (Cyprinodontidae). The Southwestern Naturalist 18(2):229-239.

Fowler, H.W. 1916. Notes on fishes of the orders Haplomi and Microcyprini. Proc. Acad. Nat. Sci. Phila. 68(3):415-439.

Gido, K. B., J. F. Schaefer, K. Work, P. W. Lienesch, E. Marsh-Matthews, and W. J. Matthews. 1999. Effects of red shiner (Cyprinella lutrensis) on Red River pupfish (Cyprinodon rubrofluviatilis). The Southwestern Naturalist 44(3):287–295.

Higgins, C.L., and G.R. Wilde. 2005. The role of salinity in structuring fish assemblages in a prairie stream system. Hydrobiologia 549:197-203.

Hill, L.G. and J.P. Holland. 1971. Preference behavior of the Red River pupfish, Cyprinodon rubrofluviatilis (Cyprinodontidae), to acclimation-salinities. The Southwestern Naturalist 16(1):55-63.

Hill, L.G., W.J. Matthews, and G. D. Schnell. 1978. Locomotor reactions to two cyprinodontid fishes to differences in dissolved oxygen concentrations. The Southwestern Naturalist 23(3):397-400.

Hubbs, C. 1957. Distributional patterns of Texas fresh-water fishes. The Southwestern Naturalist 2 (2/3):89-104.

Hubbs, C., R.J. Edwards, and G.P. Garrett. 1991. An annotated checklist of the freshwater fishes of Texas, with keys to identification of species. Texas Journal of Science, Supplement 43(4):1-56.

Matthews, W.J., K.B. Gido, G.P. Garrett, F.P. Gelwick, J.G. Stewart, and J. Schaefer. 2006. Modular experimental riffle-pool stream system. Trans. Amer. Fish. Soc. 135(6):1559-1566.

McNeely, D.L., W. Caire, A.L.N. Doss, V.M. Harris, and T. Rider. 2004. Cyprinodon rubrofluviatilis, Red River pupfish (Teleostei : Cyprinodontidae), established in the Cimarron River in Oklahoma. Southwestern Naturalist 49(1):85-87.

Miller, R.J., and H.W. Robison. 2004. Fishes of Oklahoma. University of Oklahoma Press, Norman. 450 pp.

Miller, R.R., and A.A. Echelle. 1975. Cyprinodon tularosa, a new cyprinodontid fish from the Tularosa Basin, New Mexico. The Southwestern Naturalist 19(4):365-377.

Minckley, W.L., and E.T. Arnold. 1969. “Pit-digging”, a behavioral feeding adaptation in pupfishes (Genus Cyprinodon). Journal of the Arizona Academy of Science 5:254-257.

Minckley, W.L. 1980. Cyprinodon rubrofluviatilis (Fowler), Red River pupfish. pp. 501 in D. S. Lee, et al. Atlas of North American Freshwater Fishes. N. C. State Mus. Nat. Hist., Raleigh, i-r+854 pp.

Minckley, W.L., G.K. Meffe, and D.L. Soltz. 1991. Conservation and management of short-lived fishes: the cyprinodontoids. pp. 247–282. In: W.L. Minckley & J.E. Deacon (ed.) Battle Against Extinction, Native Fish Management in the American West, The University of Arizona Press, Tucson.

Ostrand, K.G., and G.R. Wilde. 2001. Temperature, dissolved oxygen, and salinity tolerances of five prairie stream fishes and their role in explaining fish assemblage patterns. Trans. Amer. Fish. Soc. 130:742-749.

Ostrand, K.G., and G.R. Wilde. 2002. Seasonal and spatial variation in a prairie stream-fish assemblage. Ecology of Freshwater Fish 11:137-149.

Ostrand, K.G., and G.R. Wilde. 2004. Changes in prairie stream fish assemblages restricted to isolated streambed pools. Trans. Amer. Fish. Soc. 133:1329-1338.

Page, L. M. & B. M. Burr.  1991.  A field guide to freshwater fishes of North America north of Mexico.  Houghton Mifflin Company, Boston, Massachusetts. 432 pp.

Pigg, J. 1983. Three additional records for fishes rare in Oklahoma. Proc. Okla. Acad. Sci. 63:105.

Pigg, J., R. Gibbs, and G. Cottam. 1997. A record of the Red River pupfish, Cyprinodon rubrofluviatilis (Fowler), from the Salt Fork of the Arkansas River in Oklahoma. Proc. Okla. Acad. Sci. 77:122.

Pigg, J., R. Gibbs, and G.R. Luttrell. 1995. Distribution of the Red River pupfish, Cyprinodon rubrofluviatilis Fowler, in the South Canadian River in Texas and Oklahoma. Proceedings of the Oklahoma Academy of Science 75:59-60.

Pigg, J., W. Harrison, and R. Gibbs. 1984. The Red River pupfish, Cyprinodon rubrofluviatilis (Fowler), in the Arkansas River Drainage in western Oklahoma. Proc. Okla. Acad. Sci. 64:48.

Rabe, J.R., A.A. Echelle, and H.E. Schlichting. 1973. Viability of algae in the digestive tract of two cyprinodontids. Progressive Fish-Culturist 35(3):147-149.

Renfro, J.L., and L.G. Hill. 1972. Cytological adaptation in the gills of the Red River pupfish, Cyprinodon rubrofluviatilis. The Southwestern Naturalist 17(2):205-207.

Stevenson, M.M., G.D. Schnell, and R. Black. 1974. Factor analysis of fish distribution patterns in western and central Oklahoma. Systematic Zoology 23(2):202-218.

Taylor, C.M., M.R. Winston, and W.J. Matthews. 1993. Fish species-environment and abundance relationships in a Great Plains river system. Ecography 16(1):16-23.