The Case of the Red Shiner:
What Happens When a Fish Goes Bad?
 

Investigators: Noel M. Burkhead and Dane H. Huge
(Revised September 2002)

INTRODUCTION

       Of course, no species—native or not—is intrinsically "bad." However, when fishes are introduced outside their native ranges (including species native to the United States), they can cause ecological havoc.  The red shiner (Cyprinella lutrensis) is a hardy, widespread minnow native to the middle and southwestern United States and Mexico (Figure 1). Its native range encompasses the lowland tributaries of the Mississippi River and western Gulf slope drainages to the

Figure 1.  Male red shiner in near-peak spawning coloration (46 mm Standard Length).

Rio Grande River.  The red shiner peripherally occurs in the southeastern United States, inhabiting small, direct tributaries to the Mississippi River in Mississippi and Tennessee. The red shiner circumscribes the Ozark Highlands, presumably because it fairs poorly in high gradient, clear streams with relatively high species diversity.

       The red shiner is a true ecological generalist, an adaptive strategy that probably evolved during repeated exposures to desertification or extended aridity. Streams draining arid or semi-arid landscapes of the middle and southwestern U.S. are not ideal environments for most fishes, but the red shiner is just not any fish. Predominantly a denizen of creeks and small rivers, it is adapted to a wide range of environmental conditions, including seasonal intermittent flows, degraded habitats, poor water quality, and natural physiochemical extremes.  The red shiner is moderately fecund, but its realized fecundity is high due to a protracted spawning season.  While all other members of the genus Cyprinella spawn only in crevices (e.g., cracks or seams in rock, or bark fissures along submerged logs), red shiners can also broadcast or attach adhesive eggs on rocks and vegetation.  Exhibiting similar plasticity, red shiners feed throughout the water column, eating tiny crustaceans, aquatic insects, and hapless terrestrial insects that fall on water.  Red shiners seem more gregarious than other Cyprinella, which probably is the reason for it being characterized as aggressive. However, if it were toxic, the red shiner would indeed be a piscatorial Frankenstein.

       These ecological attributes predispose the red shiner to be a formidable competitor when introduced beyond its native range. It seems to establish populations wherever it has been introduced, particularly if the novel environments are degraded and have low fish diversity.

Figure 2.  Distribution of the red shiner; native range indicated by brown outline of river drainages; river drainage with introduced populations shown in red (Fuller et al. 1999.  Nonindigenous Fishes.  Special Publication Number 27, American Fisheries Society, Bethesda, MD).

The red shiner has been introduced to 11 states outside its native range (Figure 2), initially as a bait minnow, but recently, through the aquarium trade as well.  In the southeastern U.S., nonindigenous populations of red shiners occur in Alabama and Georgia (Mobile and Apalachicola river drainages), and North Carolina (Pee Dee and Roanoke river drainages).  Considering that increasing population growth is the underlying force driving aquatic habitat degradation, the future looks good for red shiners.

       In the eastern Mobile River drainage, red shiners are established in the Coosa River system in Alabama and north Georgia. A population of red shiners has been established in the Coosa River below Weiss Dam since the 1980s, in a cut-off river reach known as the "Dead River." In 1993, the red shiner was found above Weiss Reservoir in the lower Etowah River.  From this point, it had unimpeded access to most of the upper Coosa River system.  The upper Coosa River system is an aquatic Shangri-La, a veritable oasis of surviving diversity and extraordinary levels of endemism in fishes, mussels, snails, and aquatic insects. While every river is a unique ribbon of life, the Coosa River system is a riverine Eden. Here, the major upland tributaries of the Mobile River drainage, the second largest Gulf slope drainage, slip off the oldest mountains in the Southeast, creating an ancient cauldron of intense aquatic evolution.

HYBRID SWARM DISCOVERED

       Red shiner introductions have caused multiple harmful effects among native fishes, including fishes placed on the federal list of threatened and endangered species.

Figure 3.  Current distribution of the threatened blue shiner, introduced red shiner, and the hybrid (blacktail shiner X red shiner) in the upper Coosa River system, Georgia and Tennessee. The river names are: 1, Coosa River; 2, Etowah River; 3, Oostanaula River; 4, Conasauga River; 5, Coosawattee River. The first record of the red shiner in the upper Coosa River system was the 1993 capture in the lower Etowah River at mouth Dykes Creek. The brackets show dispersal of the red shiner in the Conasauga River between 2000-2001 and 2001-2002.   The upper Conasauga River is the largest of the five tributary populations that harbor blue shiners. (Larger image: 144kb .gif)

In the upper Coosa River, a system already beleaguered by an array of environmental stressors (excessive sedimentation, pollution, altered channel and bed morphology, fluctuating water levels, large impoundments), the red shiner is creating new ecological "tension."  The most obvious consequence is a hybrid swarm with a native Cyprinella species (Figure 3). The hybrid: red shiner X blacktail shiner (Cyprinella lutrensis X Cyprinella venusta stigmatura) occurs at virtually every site where red shiners occur (Figure 4). There are also three other Cyprinella species native to the system, one of which is a threatened species: the blue shiner, Cyprinella caerulea (Figure 5).

       In Summer 2000, the USGS conducted a survey of potentially rare fishes in the upper Coosa River system.  A secondary objective of that study was to determine if the red shiner had spread since 1993. The disquieting discovery was made that red shiners had dramatically expanded their range, spreading from the lower Etowah River to throughout the Oostanaula River and into the lower Conasauga and Coosawattee rivers (Figure 3). In Summer 2001, the Conasauga River was sampled again to determine if red shiner population expansion was ongoing. The small minnow had dispersed approximately 31.4 river kilometers—19.5 river miles—in one year (Figure 3).

Figure 4.  The hybrid and its parents.  Top: the blacktail shiner; middle: the hybrid; below: a male red shiner.  The intermediacy in the caudal spot and body shape are the best characters for recognizing the hybrid.

Sampling a year later in September 2002 found a single hybrid specimen (red shiner X blacktail shiner) a few miles above the upstream site in 2001.  The present upstream limits are in the portion of river between Dalton and Chattsworth, Georgia.  Interestingly, red shiners are uncommon in this river reach, particularly when compared to its relative abundance in the lower Conasauga River. However, red shiners are ensconced in a nearby, large tributary to the Conasauga River, Coahulla Creek, and have continued to spread therein (recently found in Mill Creek).  We do not know whether red shiner abundance will increase in the present upstream limits—perhaps the Coahulla Creek population will become a "source population" for future red shiner emigrations.  Or, possibly the current population levels are being limited by natural physical features, such as gradient, and the present densities of red shiners will not significantly change.  Nature is possessive; she never reveals all her secrets, but doles them out sparingly and in small helpings.

THE THREATENED BLUE SHINER

Figure 5.  The blue shiner (a male in nuptial dress).  Peak male blue shiners are uncommonly beautiful; the median fins are bright lemon yellow.

       The range of the blue shiner has been artificially fragmented into five isolated populations, the largest of which occurs in the upper Conasauga River in Georgia and Tennessee (Figure 3). If the red shiner hybridizes with the blue shiner, it could significantly reduce the reproductive success of blue shiners, and worse, possibly contaminate its gene pool. This biological threat would surely eclipse habitat degradation as the most serious threat to the blue shiner, and it would significantly increase the cost of recovery.  Worse, interactions with the red shiner could be the basis for upgrading the blue shiner to endangered status.  In September 2002, we found the lowermost blue shiner population to overlap with that of the uppermost red shiner population. Now sympatric, albeit peripherally, the stage is set to determine if laboratory experiments will in fact predict interactions in nature.

       Even if the red shiner does not hybridize with the blue shiner, it could form a "biological barrier" preventing the blue shiner from repopulating downstream from its current limits in the Conasauga River (Figure 3).  In addition, red shiners may also pose a threat to other native Cyprinella.  Where the red shiner has established, it has altered fish community composition by reducing abundance or replacing native species. Normally, native Cyprinella minnows are the dominant community members, often the top two or three species in numbers and (sometimes) biomass. How changes in community composition will affect the aquatic ecosystem is unknown.  One possible harmful consequence pertains to the reproduction of native mussels (65% of which are extinct or imperiled).  North American freshwater mussels (family Unionidae) must have a fish host for their larval stage (a glochidium) to metamorphose into a young mussel. Glochidia are expelled by gravid female mussels. Some mussel species have highly specialized anatomical structures that act as "lures," attracting inquisitive fish to the mussel.  Instead of a meal, the fish becomes host to the glochidia that attach to its fins or gills. After transformation, the young mussels drop-off the host fish, leaving it unharmed.  Some mussels have only one host fish, much like certain orchids that can only be pollinated by one insect species.  If any of the rare mussels in the upper Coosa River system require native Cyprinella for hosts, will these bivalves be able to switch to red shiners (or hybrids) as hosts? There are likely other negative effects caused by invading red shiners that are yet unknown. Biological simplification of ecosystems—through reduction or loss of native species—results in reduced "efficiencies" of processes that convert sunlight to carbon and energy-storing molecules utilized by suites of organisms.

BEHAVIORAL RESEARCH

       Research underway at the USGS Center in Gainesville is examining the interaction between reproductive red and blue shiners. The research is being conducted in "current tanks," large Plexiglas tanks (10-ft long x 4-ft wide x 2-ft deep) that use a trolling motor to generate current (Figure 6). By controlling current, water temperature, photoperiod (ratio of daylight to dark), the system mimics basic environmental features

Figure 6.  Schematic of current tanks being used to study the spawning behavior of blue and red shiners. The spawning tower, G, is a stack of acrylic plates arrayed to create the crevices in which female shiners lay eggs.  The spawning towers are easily dissembled to remove eggs for hatching in special jars.

necessary for stream spawning species.  To date, the spawning behavior of each species has been observed and extensively videotaped.  Understanding behavioral characteristics of each species, and in particular, differences between them, will help scientists understand behaviors exhibited when the two species are mixed. If the two species hybridize in the laboratory, it does not mean that hybridization will necessarily occur in nature, but it may be concluded that hybridization in nature is certainly possible.

       To date, we have observed male red shiners actively courting and spawning with female blue shiners. Indeed, we may have videotaped over a hundred such crosses.  Larvae from these cross-species spawns are presently being reared and studied to determine if hybrid larvae are present. Since hybrids are successfully produced from red shiner X blacktail shiner mixings, we doubt that developmental anomalies will preclude hybrid blue X red shiner eggs from undergoing development and normal growth.  While genetic analysis of larvae would easily reveal parentage, it would not tell the story of how the hybridization occurred.  Although study and illustration of the tiny, frail larvae is tedious, the results should enable others to identify the larvae of these species.  To date, it appears that differences in pigmentation will enable recognition of hybrid larvae of red and blue shiners.  Blue shiner larvae are illustrated in Figure 7.

       Because the spawning season of the blue shiner is relatively short, essentially the month of June, more observations are needed when territorial male blue shiners are present.  Virtually all of our observations of hybridization occurred after male blue shiners became post-nuptial

Figure 7.  Dorsal, lateral, and ventral aspects of four larval developmental stages of the blue shiner.  The distribution of pigment cells (melanophores) is distinct between blue shiner and red shiner larvae.  Hybrid larvae should be distinct from either parent species.

(i.e., between male red shiners and female blue shiners).  We do not know if hybridization would occur, with the same frequency, when territorial male blue shiners are available to challenge red shiner males, nor what the effect of different male to female ratios would to the frequency of hybrid spawns, or lastly, whether male blue shiners will actively spawn with female red shiners. It is arguable that species-isolation mechanisms first appear as behaviors, and subsequently evolve developmental or physiological barriers. These particular questions are ones we hope to address in Summer 2003.

     If there is any chance of finding some possible action that might favor blue shiners in a contact zone, it may well be discovered in their behavior.  Understanding interactions between spawning adults of the two species are likely the most important behaviors to comprehend.  In addition to the laboratory research, survey is being conducted to determine the dispersal rate and upstream limits of red shiners in the Conasauga River.

     The present research is funded through Robin Goodloe, Athens Field Office, U.S. Fish and Wildlife Service, with significant salary cost sharing by U.S.G.S. Thanks are extended to colleagues who have assisted us in the field and laboratory, and who have provided valuable comments on the problem. From the Florida Integrated Sciences Center: George Dennis, Howard L. Jelks, Robert J. Lewis, Leo Nico, Andrew Quaid, Travis Tuten, and Stephen J. Walsh. From the Institute of Ecology, University of Georgia: Byron (Bud) Freeman, Brady A. Porter, Erika Curry, Brian Nuse, Casey S. Storey, and Jesslyn Storey.

For more information, contact:
Noel Burkhead  noel_burkhead@usgs.gov
Dane Huge  dane_huge@usgs.gov