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Effects of habitat fragmentation on a stream-dwelling species, the flattened musk turtle Sternotherus depressus
Biological Conservation 54 (1990) 33~,5
Effects of Habitat Fragmentation on a Stream-dwelling Species, the Flattened Musk Turtle Sternotherus depressus C. K e n n e t h D o d d , Jr National Ecology Research Center, US Fish and Wildlife Service, 412 NE 16th Ave, Room 250, Gainesville, Florida 32601, USA (Received~9 May 1989; revised version received 27 November 1989; accepted 11 January 1990) ABSTRACT Theflattened musk turtle Sternotherus depressus has disappearedJrom more than half of its former range because of habitat modifications to stream and river channels in the Warrior River Basin, Alabama. Only 6"9% of its probable historic range contains relatively healthy populations, and most populations are j'ragmented by extensive areas of unsuitable habitat. Turtles in the best remaining habitats continue to be vulnerable to disease and human-related disturbance, collecting and habitat modification. These factors lead to population declines and abnormal population structure. Habitat fragmentation, especially in small populations, increases vulnerability to humancaused catastrophes and demographic accidents, and could lead to eventual extinction. The threats facing fragmented populations of this turtle probably parallel those affecting many other stream-dwelling species throughout the southeastern United States.
INTRODUCTION The importance of habitat fragmentation as a threat to ecosystems and species is a widely recognized problem (Whitcomb et al., 1981; Wilcove et al., 1986). Most discussions center on islands or unique continental terrestrial habitats, such as mountaintops, that are separated from distant sources of colonization (Wilcox, 1980; Temple & Cary, 1988). Isolated populations have varying probabilities of survival, depending on the taxa involved, dispersal capabilities, intervening barriers, duration of isolation, and areal extent of 33 Biol. Conserv.0006-3207/90/$03"50 © 1990 Elsevier Science Publishers Ltd, England. Printed in Great Britain
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both the isolated habitat and the source of colonizers (Wilcox & Murphy, 1985). While anthropogenic habitat fragmentation adversely affects most native terrestrial plants and animals, its importance as an isolating mechanism in stream-dwelling species has been largely overlooked. Studies on the western desert fish fauna, a major exception, show that present distributions are largely the result of fragmentation as lakes and rivers dried throughout the Pleistocene (Hubbs & Miller, 1948; Soltz & Naiman, 1978). Within the last 40 years, however, demand for agricultural and municipal water has accelerated fragmentation to the point that many extant desert fish populations are threatened, and require intensive management to survive (Meffe & Vrijenhoek, 1988). Fragmentation also has contributed to the endangered status of Colorado River fishes as that system has been dammed for hydroelectric and flood control projects (Ono et al., 1983). The flattened musk turtle Sternotherus depressus is an aquatic, bottomdwelling species endemic to streams of the Warrior River Basin of northcentral Alabama (Mount, 1975). Prior to 1985, two studies were conducted on its status and distribution in connection with a review of its status as a threatened species under provisions of the US Endangered Species Act of 1973 (US Fish and Wildlife Service, 1987). While these studies reached different conclusions regarding the species' status, both studies recognized significant threats to the turtle's existence. During the summer of 1985, 10 streams were systematically sampled to determine the effects of habitat degradation related to coal mining on the distribution, abundance and population structure of S. depressus (Dodd et al., 1988). As fieldwork progressed, the extent to which populations of this species were physically isolated from one another by extensive areas of unfavorable habitat became increasingly apparent. Subsequent data analysis, information received during public hearings, and fieldwork conducted in 1986 supported these initial impressions (Dodd, 1988, 1989; D o d d e t al., 1988). Although it has not been possible to sample intensively all stream segments in the Warrior River Basin, a comparative analysis using data from past studies should allow biologically reasonable scenarios to be advanced concerning the effects of habitat fragmentation on this species. Here, I present new data on the extent of the turtle's remaining habitat and discuss threats posed by fragmentation.
STUDY AREA A N D METHODS The Warrior River Basin comprises approximately 16 174km z in north central Alabama. The area is part of the Cumberland Plateau Physiographic
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Province, and the land is a peneplain dissected by rivers and streams producing many gorges in the Pennsylvanian Age sandstone. The major river within the range of the flattened musk turtle is the Warrior (or Black Warrior) River containing a drainage area of approximately 10 308 km 2 above Bankhead Dam. The three major tributaries are Locust, Mulberry and Sipsey Forks. Within the range of S. depressus, major impoundments are Bankhead Lake, completed more than 65 years ago, the lake behind Holt Dam, completed in 1968, and Lewis Smith Lake, completed in 1961. In addition, there are a number of lesser dams on various tributaries, such as Brushy Creek Lake on Brushy Creek and Inland Lake on Blackburn Fork. The Warrior Basin includes the most productive of Alabama's three coalmining regions, the Warrior Coal Basin (Tolson, 1984). This basin underlies a substantial portion of the range of S. depressus, and strip mining for coal has led to widespread siltation and pollution of streams. The streams also have been heavily affected by agricultural runoff, pollution and sewage discharge from various municipalities, particularly Warrior, Jasper, and Birmingham, and from improper streambank management (Dodd et al., 1988). Water pollution has adversely affected the fishery resources throughout the Warrior River Basin (US Fish and Wildlife Service, 1987). Descriptions of study sites, criteria for site selection, collecting methods, and results of surveys conducted in 1985 and 1986 are published elsewhere (Dodd et al., 1988; Dodd, 1988, 1989). The collecting results from unpublished studies (R. Mount, and C. Ernst, K. Marion and F. Cox; see US Fish and Wildlife Service, 1987) were plotted on US Geological Survey (USGS) 1 : 250 000 topographical maps. I examined sites trapped by previous workers and looked at nearby streams as potential S. depressus habitat. As a result of an examination of unpublished data on status and distribution, field observations in 1985 and 1986, trapping results, and water quality analysis (Dodd et al., 1988), stream segments in the Warrior Basin above Bankhead Dam, i.e. areas lacking hybridization with the related Sternotherus minor (Iverson, 1977), were assigned to one of four categories based on the status of the S. depressus population at that locality. Stream order classification is based on criteria in Kuehne (1962). Category 1 streams had viable S. depressus populations and included larger streams with drainage areas generally > 120kin 2, a stream order of 3 or 4, no obvious signs of heavy siltation and pollution, good habitat conditions (Dodd et al., 1988), and trap catch ratios better than one turtle per 65 trap hours. Category 2 included streams with depleted turtle populations. These streams also had drainage areas > 120 km 2 and stream orders of 3 and 4, but had heavy siltation from agriculture, municipal, or mining activities, poor habitat conditions, or poor trap catch ratios (one turtle in more than 65 trap hours). Occasional stream sections were included in category 2 if good
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habitat conditions were present but interspersed with poor habitat conditions, or if catch success ratios were < 1:65 in one study but > 1:65 in a later study (e.g. Turkey Creek). Category 3 streams contained segments with extirpated flattened musk turtle populations. This category included those stream segments that, because of their size (stream orders 3 and 4), probably lost turtle populations because of pollution (e.g. Valley and Village Creeks), and those sections of major rivers now impounded. Although occasional flattened musk turtles may enter the upper reaches of certain impoundments (R. Mount and C. Ernst, pers. comm.), there is no indication that the species is lacustrine as is its sympatric congener Sternotherus odoratus. Category 4 streams had drainage areas generally less than 120 km 2 or were otherwise likely to be too small (stream orders 1 and 2) to contain S. depressus populations. The exact size at which upstream fragmentation occurs for an otherwise contiguous population of S. depressus is unknown, so this point was set somewhat arbitrarily. In other turtles, the limit of upstream distribution is related to the difficulty of dispersal, patchiness of favorable habitat and changing environmental conditions (Shively & Jackson, 1985). The status of flattened musk turtle populations in each stream section was color-coded on a drainage map of the Warrior Basin. The linear extent of stream habitat within each of the four status categories was then derived using a Calcomp Model 9000 digitizer.
EXTENT OF R E M A I N I N G HABITAT Many streams in the Warrior River Basin are small and probably never supported populations of the flattened musk turtle (Fig. I(A); category 4, totaling approximately 686-7km on the prepared maps). These streams included the headwaters of major streams and rivers, such as Sipsey, Locust and Mulberry Forks, and small tributary streams to the larger rivers. The remaining three categories totaled 1870.4 km, including all stream segments that presumably once supported populations of flattened musk turtles. Category 1 streams (Fig. I(B) comprised only 60km (6-9% of suitable habitat), and included Sipsey Fork and Brushy Creek above Lewis Smith Lake, Blackwater Creek below the Musgrove Country Club Dam, and Blackburn Fork below Inland Lake. These streams are the only remaining habitats within the Warrior River Basin relatively free of siltation, and constitute critical habitats for S. depressus. Category 2 streams comprised 321.3 km (36.9%) of remaining habitat,
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including the main channels of Locust and Mulberry Forks, as well as the downstream sections of major tributaries such as Gurley and Turkey PCreeks (Fig. I(C). The main channels of these large streams carry heavy sediment loads from strip mines that line the riverbanks, municipal runoff from towns and cities, and agricultural runoff. These streams contain S. depressus, and it is unlikely that the species can persist in them if sediments continue to reduce cover and gastropod mollusk populations, the turtle's principal food source. In the tributaries, Dodd et al. (1988) determined that the distribution often was not contiguous (e.g. Turkey and Gurley Creeks), but that microdistribution reflected variation in patterns of sedimentation, cover and water current. Category 3 river segments made up the greatest length (490" 1 km, 56.3 %) of potential habitat in the Warrior River Basin (Fig. I(D)) because large amounts of main stream channel were flooded by major impoundments on the Warrior River and Sipsey Fork, thus eliminating much optimum turtle habitat. Sections of tributary streams such as Lost and Blackwater Creeks, as well as nearly all of Cane and Wolf Creeks, were included in this category because of severe habitat degradation from a variety of sources, notably strip mining.
Habitat fragmentation: Causes Habitat fragmentation of turtle populations in the Warrior River Basin results primarily from three sources, sedimentation, impoundments and pollution. Sedimentation results from chronic and uncontrolled runoff from strip mines, many of which date to the 1940s and earlier (Dodd et al., 1988), agricultural fields, improper streambank management and construction projects adjacent to the stream. Sediments, particularly of coal fines from adjacent strip mines, are often > 1 m deep and may clog crevices and potential cover sites for many kilometers downstream from their point of entry, depending on stream size. Impoundments create deep lentic waters not suitable for this stream-dwelling species. Pollution from urban runoff and chemical discharge has eliminated many aquatic vertebrates and invertebrates from streams in the Warrior River Basin, particularly those streams draining the Birmingham metropolitan area (e.g. Valley and Village Creeks). These factors eliminate turtles either through direct effects, such as loss of crevice and other narrow cover sites (Jackson, 1988), or indirectly, such as by adversely affecting mollusk populations. Within the Warrior River Basin, each source has created extensive patches of unoccupied habitat that were once inhabited by flattened musk turtles (Fig. 1).
.t
Fig. 1. Drainage map of the upper Warrior Basin showing the distribution of the flattened musk turtle. (11) sampling locations with turtles; (O) sampling locations where turtles have not been collected; D, data reported in Dodd et al. (1988); E, data from C. Ernst, K. Marion and F. Cox (pers. comm.); M, data from R. Mount (pers. comm.). (A) Distribution of headwater streams. (B) Stream segments with viable turtle populations.
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iA
Fig. 1--contd. (C) Stream segments with small or reduced populations affected by habitat degradation. (D) Areas lacking permanent S. depressus populations.
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An example of habitat fragmentation: Lost Creek Lost Creek drains an area of nearly 900 km 2, arising from headwaters near Carbon Hill, Walker County. It flows generally southeast until it joins Mulberry Fork. Strip mines border the stream throughout nearly its entire length, resulting in massive siltation from near the former town of Holly Grove downstream to its junction with Mulberry Fork. Further downstream, the stream becomes muddier and more lentic. Flattened musk turtles are now known to occur only in three isolated stream sections, one near the headwaters (Dodd et al., 1988), one in the backwaters and below the mill dam near Cedrum, and one approximately 6"3 km southeast of Cedrum. At maximum, these sections comprise a linear extent of 41.67 km of available habitat. At least 23 km of habitat (55-2% of historically available habitat) have now been so severely degraded that the flattened musk turtle is extirpated. At the upstream segment, > 2700 h of trapping and wading from April through September 1985 yielded only 5 large males, 6 large females, and one hatchling (Dodd et al., 1988). In 1989, Robert Mount (pers. comm.) trapped and waded this section and was unsuccessful in catching any turtles. The lack of large juveniles and small adults suggests that there is no successful recruitment. At the site near Cedrum, C. Ernst, K. Marion and F. Cox (pers. comm.) collected 11 adults of varying size classes, and considered the population 'moderate to high'. However, the linear extent of habitat is generally limited upstream by the Cedrum mill dam, although a few turtles have been recently (1989) observed in the dam's backwater (R. Mount, pers. comm.), and downstream by extensive strip-mine discharge. At the farthest downstream site, R. Mount (pers. comm.) found basking flattened musk turtles between McLain Bridge and Tubbs Bridge during a 1989 survey. These basking turtles exhibited similar disease symptoms to those reported by Dodd (1988) at Sipsey Fork. It is possible that there could be interchange between the populations of flattened musk turtles in Lost Creek because turtle movements in unimpeded stream sections may exceed 400 m ( D o d d e t al., 1988). However, it is unlikely that individuals could find their way through several kilometers of deep reservoirs and around dams. Successful movements through the lower reaches of Lost Creek to favorable habitats in other drainages are unlikely because they would require a move of > 15km to a dammed portion of Mulberry Fork, thence upstream another 25-30 km through the backwaters of Bankhead Lake. A straight-line overland movement of approximately 10kin to the north would put an individual in favorable habitat, but a railroad and several major roads would have to be crossed. Thus, flattened musk turtles in Lost Creek are almost certainly isolated from
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other populations, and there is probably no interchange between the three surviving populations, one of which is already small and shows no successful recruitment. This scenario is probably similar to that in other stream segments in the basin.
Threats to fragmented populations Once isolated, populations of S. depressus and other stream-dwelling turtles may be subject to a wide variety of natural and human-induced threats to their existence. In addition to the potential loss of genetic viability and heterozygosity in small fragmented populations, threats to S. depressus include: (1)
Small population size/abnormal population structure. Some flattened musk turtle populations (e.g. Gurley Creek) are composed of only a few large old individuals. In other populations, adults are common, but the absence of large juveniles or small adults (e.g. Turkey Creek) indicates no recent recruitment. Also, the sex ratio may be substantially skewed (Dodd, 1989). Because similar collecting methods and effort were used to sample all populations (Dodd et al., 1988), variation in population structure probably reflects the extent that various factors, including fragmentation, are affecting the population. Small populations are particularly vulnerable to both natural and human-caused perturbations. Even without direct external threats, such populations are vulnerable to stochastic events because of small size (Franklin, 1980; Soul6 & Simberloff, 1986; Pimm et al., 1988) and should be monitored closely.
(2) Disease. The largest population of S. depressus occurs upstream of Lewis Smith Lake in Sipsey Fork (Dodd et al., 1988). Presumably, this population is isolated from populations downstream by the reservoir. In 1985, a disease of unknown etiology struck this population, and the population declined by 50% within one season (Dodd, 1988). Although the population decline could not be solely attributed to disease, the vulnerability of small isolated igopulations to disease should be obvious. Turtles with disease symptoms have been observed in the Brushy Creek, and may be present in the downstream population in Lost Creek. (3)
Collecting. Easy access to collecting locations, docile disposition, attractiveness of individual turtles and rarity have combined to create a substantial demand for S. depressus before federal protection (US Fish and Wildlife Service, 1987). As many as 200 individuals may have been collected during July 1985 at Sipsey Fork (Dodd et al.,
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1988). Collectors also removed turtles in substantial numbers from other localities, and the lack of large adults in Blackwater Creek and of non-pitted small adults in Blackburn Fork is presumably the result of collecting pressure (Dodd et al., 1988).
CONCLUSIONS Through the process of stream capture (e.g. Lachner & Jenkins, 1971, for the fish Nocomis micropogon), geologic uplifts, glaciation and sea level fluctuations, natural fragmentation of drainage systems throughout the southeastern United States has led to repeated opportunities for colonization and speciation as streams were alternately connected and isolated. Barriers such as the Fall Line and the falls on the Kanawha River sometimes led to different faunas in upstream and downstream habitats or to the isolation of populations of widely ranging species (Tinkle, 1959; Jenkins et al., 1971; Hocutt et al., 1979; Seidel, 1981). As a result, there is a high degree of endemism and species richness for many taxa in drainages of the Southeast and Interior Low Plateau regions of the United States, particularly in rivers draining into the Gulf of Mexico (Ernst & Barbour, 1972; Branson, 1985; Fitzpatrick, 1986). Congeneric taxa often occupy adjacent drainages (e.g. the turtle genus Graptemys, Ernst & Barbour, 1972), and chromosomal and phenotypic differentiation often occurs among populations of a single species inhabiting adjacent drainages (Chambers, 1980, 1982; Bermingham & Avise, 1986). The habitat fragmentation occurring today is not related to change occurring in a geologic time scale. Instead, fragmentation results from direct modifications (e.g. channelization, dam construction, pulling snags used as aquatic turtle basking platforms) that in an ecological sense are instantaneous. Adverse modification of water quality also may be instantaneous (e.g. chemical spills), or may occur gradually over a longer time (e.g. siltation and sewage discharge). All contribute to the insularization of the diverse stream biota of southeastern North America. Adverse stream channel modification already has eliminated many mollusks (Stansbery, 1976; Stein, 1976) and fishes (e.g. Etnier et al., 1979), has altered native fish species composition (Timmons, 1982), and may be contributing to the decline of additional turtle species (US Fish and Wildlife Service, 1986). Sheldon (1988) suggested the importance of habitat fragmentation to stream faunas by presenting the analogy of rivers as archipelagos. In addition to being insular (i.e. between drainages), physical barriers on rivers, both natural and human-created, partition aquatic habitats into a series of
Turtle habitat fragmentation
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archipelagos. Although there is no way of knowing the extent of natural within-stream insularization for most taxa in aquatic habitats, humancreated fragmentation should force a reassessment of streams and rivers as contiguous habitats. The fragmentation of S. depressus habitat and the concomitant threats to its remaining populations dramatize the status of much of the freshwater stream biota throughout the southeastern and south-central United States. Immediate research needs to identify the microdistribution and status of this fauna, monitor changes in populations already known to be fragmented, and suggest ways to ameliorate both present and future deleterious effects of fragmentation. A C K N O W L E D G E M ENTS I thank Kevin Enge and James Stuart for field assistance. Bert Charest prepared Fig. 1. Robert Mount provided new information on Lost Creek turtles. Gary Meffe, Paul Opler and James D. Williams provided comments on various versions of the manuscript. Fieldwork was supported by a grant from the Office of Surface Mining, US Department of the Interior, and the Endangered Species Program, US Fish and Wildlife Service. These surveys were conducted under scientific collecting permits No. 172 and 259 from the Alabama Department of Conservation.
REFERENCES Bermingham, E. & Avise, J. C. (1986). Molecular zoogeography of freshwater fishes of the southeastern United States. Genetics, 113, 939-65. Branson, B. A. (1985). Aquatic distributional patterns in the Interior Lowland Plateau. Brimleyana, 11, 169-89. Chambers, S. M. (1980). Genetic divergence between populations of Goniobasis (Pleuroceridae) occupying different drainage systems. Malacologia, 20, 63-81. Chambers, S. M. (1982). Chromosomal evidence for parallel evolution of shell sculpture pattern in Goniobasis. Evolution, 36, 113-20. Dodd, C. K., Jr (1988). Disease and population declines in the flattened musk turtle Sternotherus depressus. Am. Midl. Nat., 119, 394-401. Dodd, C. K., Jr (1989). Secondary sex ratio variation among populations of the flattened musk turtle Sternotherus depressus. Copeia, 1989, 1041-5. Dodd, C. K., Jr, Enge, K. M. & Stuart, J. N. (1988). Aspects of the biology of the flattened musk turtle, Sternotherus depressus in northern Alabama. Bull. Florida St. Mus., Biol. Sci., 34, 1-64. Ernst, C. H. & Barbour, R. W. (1972). Turtles of the United States. University Press of Kentucky, Lexington. Etnier, D. A., Starnes, W. C. & Bauer, B. H. (1979). Whatever happened to the silvery
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minnow (Hybognathus nuchalis) in the Tennessee River? S.E. Fish. Counc. Proc., 2, 1-3. Fitzpatrick, J. F., Jr (1986). The pre-Pliocene Tennessee River and its bearing on crawfish distribution (Decapoda: Cambaridae). Brimleyana, 12, 123-46. Franklin, I. R. (1980). Evolutionary change in small populations. In Conservation Biology. An Evolutionary-Ecological Perspective, ed. M. E. Soul6 & B. A. Wilcox. Sinauer Associates, Inc., Sunderland, Massachusetts, pp. 135-49. Hocutt, C. H., Denoncourt, R. F. & Stauffer, J. R., Jr (1979). Fishes of the Gauley River, West Virginia. Brimleyana, 1, 47-80. Hubbs, C. L. & Miller, R. R. (1948). The zoological evidence: Correlation between fish distribution and hydrographic history in the desert basins of western United States. In The Great Basin, with Emphasis on Glacial and Postglacial Times. Bull. Univ. Utah, 38, 17-166. Iverson, J. B. (1977). Geographic variation in the musk turtle Sternotherus minor. Copeia, 1977, 502-17. Jackson, J. F. (1988). Crevice occupation by musk turtles: taxonomic distribution and crevice attributes. Anim. Behav., 36, 793-801. Jenkins, R. E., Lachner, E. A. & Schwartz, F. J. (1971). Fishes of the central Appalachian drainages: Their distribution and dispersal. In The Distributional History of the Biota of the Southern Appalachians, Part 111: Vertebrates, ed. P. C. Holt. VPI & State University, Blacksburg, Res. Div. Monogr. No. 4, 43-117. Kuehne, R. (1962). The classification of streams, illustrated by fish distribution in an eastern Kentucky creek. Ecology, 43, 608-14. Lachner, E. A. & Jenkins, R. E. (1971). Systematics, distribution and evolution of the chub genus Nocomis Girard (Pisces, Cyprinidae) of eastern United States, with descriptions of new species. Smithson. Contrib. Zool., 85, 1-97. Meffe, G. K. & Vrijenhoek, R. C. (1988). Conservation genetics in the management of desert fishes. Conserv. BioL, 2, 157-69. Mount, R. H. (1975). The Reptiles & Amphibians of Alabama. Agricultural Experiment Station, Auburn University, Auburn, Alabama. Ono, R. D., Williams, J. D. & Wagner, A. (1983). Vanishing Fishes of North America. Stone Wall Press, Washington, DC. Pimm, S. L., Jones, H. L. & Diamond, J. (1988). On the risk of extinction. Am. Nat., 132, 757-85. Seidel, M. E. (1981). A taxonomic analysis of pseudemyd turtles (Testudines: Emydidae) from the New River, and phenetic relationships in the subgenus Pseudemys. Brimleyana, 6, 25-44. Sheldon, A. L. (1988). Conservation of stream fishes: Patterns of diversity, rarity, and risk. Conserv. Biol., 2, 149-56. Shively, S. H. & Jackson, J. F. (1985). Factors limiting the upstream distribution of the Sabine map turtle. Am. Midl. Nat., 114, 292-303. Soltz, D. L. & Naiman, R. J. (1978). The natural history of native fishes in the Death Valley system. Nat. Hist. Mus. Los Angeles Cty, Sci. Ser., 30, 1-76. Soul6, M. E. & Simberloff, D. S. (1986). What do genetics and ecology tell us about the design of nature reserves? Biol. Conserv., 35, 19-40. Stansbery, D. H. (1976). Naiad mollusks. In Endangered and Threatened Plants and Animals of Alabama, ed. H. Boschung. Bull. Alabama Mus. Nat. Hist., 2, 42-52. Stein, C. B. (1976). Gastropods. In Endangered and Threatened Plants andAnimals of Alabama, ed. H. Boschung. Bull, Alabama Mus. Nat. Hist., 2, 21-41.
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Temple, S. A. & Cary, J. R. (1988). Modeling dynamics of habitat-interior bird populations in fragmented landscapes. Conserv. Biol., 2, 340-47. Timmons, T. J. (1982). Initial changes in fish species composition in two new lakes of the Tennessee-Tombigbee waterway, Alabama-Mississippi. S.E. Fish. Count. Proc., 4, 1-4. Tinkle, D. W. (1959). The relation of the Fall Line to the distribution and abundance of turtles. Copeia, 1959, 167 70. Tolson, J. S. (1984). Alabama coal data for 1983. Geol. Surv. Alabama, hTf~rmatioH Ser., 58E, Tuscaloosa, Alabama. US Fish and Wildlife Service (1986). Determination of threatened status tbr the ringed sawback turtle (Graptemys oculifera). Fed. Reg., 51, 45908 10. US Fish and Wildlife Service (1987). Determination of threatened status t~r the flattened musk turtle (Sternotherus depressus). Fed. Reg., 52, 22418-30. Wilcove, D. S., McLellan, C. H. & Dobson, A. P. (1986). Habitat fragmentation in the Temperate Zone. In Conservation Biology. The Science of Scarcity and Diversity, ed. M. E. Soul6. Sinauer Associates, Inc., Sunderland, Massachussetts, pp. 237-56. Wilcox, B. A. (1980). Insular ecology and conservation. In Conservation Bioloey. A n Evolutionary-Ecological Perspective, ed. M. E. Soul6 & B, A. Wilcox. Sinauer Associates, Inc., Sunderland, Massachusetts, pp. 95-117. Wilcox, B. A. & Murphy, D. D. (1985). Conservation strategy: the effects of fragmentation on extinction. Am. Nat., 125, 879 87. Whitcomb, R. F., Robbins, C. S., Lynch, J. F., Whitcomb, B. L., Klimkiewicz, M. K. & Bystrak, D. (1981). Effects of forest fragmentation on avifauna of the eastern deciduous forest. In Forest Island Dynamics in Man-Dominated Landscapes, ed. R. L. Burgess & D. M. Sharpe. Springer-Verlag, New York, pp. 125 292.
Effects of Habitat Fragmentation on a Stream-dwelling Species, the Flattened Musk Turtle Sternotherus depressus C. K e n n e t h D o d d , Jr National Ecology Research Center, US Fish and Wildlife Service, 412 NE 16th Ave, Room 250, Gainesville, Florida 32601, USA (Received~9 May 1989; revised version received 27 November 1989; accepted 11 January 1990) ABSTRACT Theflattened musk turtle Sternotherus depressus has disappearedJrom more than half of its former range because of habitat modifications to stream and river channels in the Warrior River Basin, Alabama. Only 6"9% of its probable historic range contains relatively healthy populations, and most populations are j'ragmented by extensive areas of unsuitable habitat. Turtles in the best remaining habitats continue to be vulnerable to disease and human-related disturbance, collecting and habitat modification. These factors lead to population declines and abnormal population structure. Habitat fragmentation, especially in small populations, increases vulnerability to humancaused catastrophes and demographic accidents, and could lead to eventual extinction. The threats facing fragmented populations of this turtle probably parallel those affecting many other stream-dwelling species throughout the southeastern United States.
INTRODUCTION The importance of habitat fragmentation as a threat to ecosystems and species is a widely recognized problem (Whitcomb et al., 1981; Wilcove et al., 1986). Most discussions center on islands or unique continental terrestrial habitats, such as mountaintops, that are separated from distant sources of colonization (Wilcox, 1980; Temple & Cary, 1988). Isolated populations have varying probabilities of survival, depending on the taxa involved, dispersal capabilities, intervening barriers, duration of isolation, and areal extent of 33 Biol. Conserv.0006-3207/90/$03"50 © 1990 Elsevier Science Publishers Ltd, England. Printed in Great Britain
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both the isolated habitat and the source of colonizers (Wilcox & Murphy, 1985). While anthropogenic habitat fragmentation adversely affects most native terrestrial plants and animals, its importance as an isolating mechanism in stream-dwelling species has been largely overlooked. Studies on the western desert fish fauna, a major exception, show that present distributions are largely the result of fragmentation as lakes and rivers dried throughout the Pleistocene (Hubbs & Miller, 1948; Soltz & Naiman, 1978). Within the last 40 years, however, demand for agricultural and municipal water has accelerated fragmentation to the point that many extant desert fish populations are threatened, and require intensive management to survive (Meffe & Vrijenhoek, 1988). Fragmentation also has contributed to the endangered status of Colorado River fishes as that system has been dammed for hydroelectric and flood control projects (Ono et al., 1983). The flattened musk turtle Sternotherus depressus is an aquatic, bottomdwelling species endemic to streams of the Warrior River Basin of northcentral Alabama (Mount, 1975). Prior to 1985, two studies were conducted on its status and distribution in connection with a review of its status as a threatened species under provisions of the US Endangered Species Act of 1973 (US Fish and Wildlife Service, 1987). While these studies reached different conclusions regarding the species' status, both studies recognized significant threats to the turtle's existence. During the summer of 1985, 10 streams were systematically sampled to determine the effects of habitat degradation related to coal mining on the distribution, abundance and population structure of S. depressus (Dodd et al., 1988). As fieldwork progressed, the extent to which populations of this species were physically isolated from one another by extensive areas of unfavorable habitat became increasingly apparent. Subsequent data analysis, information received during public hearings, and fieldwork conducted in 1986 supported these initial impressions (Dodd, 1988, 1989; D o d d e t al., 1988). Although it has not been possible to sample intensively all stream segments in the Warrior River Basin, a comparative analysis using data from past studies should allow biologically reasonable scenarios to be advanced concerning the effects of habitat fragmentation on this species. Here, I present new data on the extent of the turtle's remaining habitat and discuss threats posed by fragmentation.
STUDY AREA A N D METHODS The Warrior River Basin comprises approximately 16 174km z in north central Alabama. The area is part of the Cumberland Plateau Physiographic
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Province, and the land is a peneplain dissected by rivers and streams producing many gorges in the Pennsylvanian Age sandstone. The major river within the range of the flattened musk turtle is the Warrior (or Black Warrior) River containing a drainage area of approximately 10 308 km 2 above Bankhead Dam. The three major tributaries are Locust, Mulberry and Sipsey Forks. Within the range of S. depressus, major impoundments are Bankhead Lake, completed more than 65 years ago, the lake behind Holt Dam, completed in 1968, and Lewis Smith Lake, completed in 1961. In addition, there are a number of lesser dams on various tributaries, such as Brushy Creek Lake on Brushy Creek and Inland Lake on Blackburn Fork. The Warrior Basin includes the most productive of Alabama's three coalmining regions, the Warrior Coal Basin (Tolson, 1984). This basin underlies a substantial portion of the range of S. depressus, and strip mining for coal has led to widespread siltation and pollution of streams. The streams also have been heavily affected by agricultural runoff, pollution and sewage discharge from various municipalities, particularly Warrior, Jasper, and Birmingham, and from improper streambank management (Dodd et al., 1988). Water pollution has adversely affected the fishery resources throughout the Warrior River Basin (US Fish and Wildlife Service, 1987). Descriptions of study sites, criteria for site selection, collecting methods, and results of surveys conducted in 1985 and 1986 are published elsewhere (Dodd et al., 1988; Dodd, 1988, 1989). The collecting results from unpublished studies (R. Mount, and C. Ernst, K. Marion and F. Cox; see US Fish and Wildlife Service, 1987) were plotted on US Geological Survey (USGS) 1 : 250 000 topographical maps. I examined sites trapped by previous workers and looked at nearby streams as potential S. depressus habitat. As a result of an examination of unpublished data on status and distribution, field observations in 1985 and 1986, trapping results, and water quality analysis (Dodd et al., 1988), stream segments in the Warrior Basin above Bankhead Dam, i.e. areas lacking hybridization with the related Sternotherus minor (Iverson, 1977), were assigned to one of four categories based on the status of the S. depressus population at that locality. Stream order classification is based on criteria in Kuehne (1962). Category 1 streams had viable S. depressus populations and included larger streams with drainage areas generally > 120kin 2, a stream order of 3 or 4, no obvious signs of heavy siltation and pollution, good habitat conditions (Dodd et al., 1988), and trap catch ratios better than one turtle per 65 trap hours. Category 2 included streams with depleted turtle populations. These streams also had drainage areas > 120 km 2 and stream orders of 3 and 4, but had heavy siltation from agriculture, municipal, or mining activities, poor habitat conditions, or poor trap catch ratios (one turtle in more than 65 trap hours). Occasional stream sections were included in category 2 if good
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habitat conditions were present but interspersed with poor habitat conditions, or if catch success ratios were < 1:65 in one study but > 1:65 in a later study (e.g. Turkey Creek). Category 3 streams contained segments with extirpated flattened musk turtle populations. This category included those stream segments that, because of their size (stream orders 3 and 4), probably lost turtle populations because of pollution (e.g. Valley and Village Creeks), and those sections of major rivers now impounded. Although occasional flattened musk turtles may enter the upper reaches of certain impoundments (R. Mount and C. Ernst, pers. comm.), there is no indication that the species is lacustrine as is its sympatric congener Sternotherus odoratus. Category 4 streams had drainage areas generally less than 120 km 2 or were otherwise likely to be too small (stream orders 1 and 2) to contain S. depressus populations. The exact size at which upstream fragmentation occurs for an otherwise contiguous population of S. depressus is unknown, so this point was set somewhat arbitrarily. In other turtles, the limit of upstream distribution is related to the difficulty of dispersal, patchiness of favorable habitat and changing environmental conditions (Shively & Jackson, 1985). The status of flattened musk turtle populations in each stream section was color-coded on a drainage map of the Warrior Basin. The linear extent of stream habitat within each of the four status categories was then derived using a Calcomp Model 9000 digitizer.
EXTENT OF R E M A I N I N G HABITAT Many streams in the Warrior River Basin are small and probably never supported populations of the flattened musk turtle (Fig. I(A); category 4, totaling approximately 686-7km on the prepared maps). These streams included the headwaters of major streams and rivers, such as Sipsey, Locust and Mulberry Forks, and small tributary streams to the larger rivers. The remaining three categories totaled 1870.4 km, including all stream segments that presumably once supported populations of flattened musk turtles. Category 1 streams (Fig. I(B) comprised only 60km (6-9% of suitable habitat), and included Sipsey Fork and Brushy Creek above Lewis Smith Lake, Blackwater Creek below the Musgrove Country Club Dam, and Blackburn Fork below Inland Lake. These streams are the only remaining habitats within the Warrior River Basin relatively free of siltation, and constitute critical habitats for S. depressus. Category 2 streams comprised 321.3 km (36.9%) of remaining habitat,
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including the main channels of Locust and Mulberry Forks, as well as the downstream sections of major tributaries such as Gurley and Turkey PCreeks (Fig. I(C). The main channels of these large streams carry heavy sediment loads from strip mines that line the riverbanks, municipal runoff from towns and cities, and agricultural runoff. These streams contain S. depressus, and it is unlikely that the species can persist in them if sediments continue to reduce cover and gastropod mollusk populations, the turtle's principal food source. In the tributaries, Dodd et al. (1988) determined that the distribution often was not contiguous (e.g. Turkey and Gurley Creeks), but that microdistribution reflected variation in patterns of sedimentation, cover and water current. Category 3 river segments made up the greatest length (490" 1 km, 56.3 %) of potential habitat in the Warrior River Basin (Fig. I(D)) because large amounts of main stream channel were flooded by major impoundments on the Warrior River and Sipsey Fork, thus eliminating much optimum turtle habitat. Sections of tributary streams such as Lost and Blackwater Creeks, as well as nearly all of Cane and Wolf Creeks, were included in this category because of severe habitat degradation from a variety of sources, notably strip mining.
Habitat fragmentation: Causes Habitat fragmentation of turtle populations in the Warrior River Basin results primarily from three sources, sedimentation, impoundments and pollution. Sedimentation results from chronic and uncontrolled runoff from strip mines, many of which date to the 1940s and earlier (Dodd et al., 1988), agricultural fields, improper streambank management and construction projects adjacent to the stream. Sediments, particularly of coal fines from adjacent strip mines, are often > 1 m deep and may clog crevices and potential cover sites for many kilometers downstream from their point of entry, depending on stream size. Impoundments create deep lentic waters not suitable for this stream-dwelling species. Pollution from urban runoff and chemical discharge has eliminated many aquatic vertebrates and invertebrates from streams in the Warrior River Basin, particularly those streams draining the Birmingham metropolitan area (e.g. Valley and Village Creeks). These factors eliminate turtles either through direct effects, such as loss of crevice and other narrow cover sites (Jackson, 1988), or indirectly, such as by adversely affecting mollusk populations. Within the Warrior River Basin, each source has created extensive patches of unoccupied habitat that were once inhabited by flattened musk turtles (Fig. 1).
.t
Fig. 1. Drainage map of the upper Warrior Basin showing the distribution of the flattened musk turtle. (11) sampling locations with turtles; (O) sampling locations where turtles have not been collected; D, data reported in Dodd et al. (1988); E, data from C. Ernst, K. Marion and F. Cox (pers. comm.); M, data from R. Mount (pers. comm.). (A) Distribution of headwater streams. (B) Stream segments with viable turtle populations.
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iA
Fig. 1--contd. (C) Stream segments with small or reduced populations affected by habitat degradation. (D) Areas lacking permanent S. depressus populations.
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An example of habitat fragmentation: Lost Creek Lost Creek drains an area of nearly 900 km 2, arising from headwaters near Carbon Hill, Walker County. It flows generally southeast until it joins Mulberry Fork. Strip mines border the stream throughout nearly its entire length, resulting in massive siltation from near the former town of Holly Grove downstream to its junction with Mulberry Fork. Further downstream, the stream becomes muddier and more lentic. Flattened musk turtles are now known to occur only in three isolated stream sections, one near the headwaters (Dodd et al., 1988), one in the backwaters and below the mill dam near Cedrum, and one approximately 6"3 km southeast of Cedrum. At maximum, these sections comprise a linear extent of 41.67 km of available habitat. At least 23 km of habitat (55-2% of historically available habitat) have now been so severely degraded that the flattened musk turtle is extirpated. At the upstream segment, > 2700 h of trapping and wading from April through September 1985 yielded only 5 large males, 6 large females, and one hatchling (Dodd et al., 1988). In 1989, Robert Mount (pers. comm.) trapped and waded this section and was unsuccessful in catching any turtles. The lack of large juveniles and small adults suggests that there is no successful recruitment. At the site near Cedrum, C. Ernst, K. Marion and F. Cox (pers. comm.) collected 11 adults of varying size classes, and considered the population 'moderate to high'. However, the linear extent of habitat is generally limited upstream by the Cedrum mill dam, although a few turtles have been recently (1989) observed in the dam's backwater (R. Mount, pers. comm.), and downstream by extensive strip-mine discharge. At the farthest downstream site, R. Mount (pers. comm.) found basking flattened musk turtles between McLain Bridge and Tubbs Bridge during a 1989 survey. These basking turtles exhibited similar disease symptoms to those reported by Dodd (1988) at Sipsey Fork. It is possible that there could be interchange between the populations of flattened musk turtles in Lost Creek because turtle movements in unimpeded stream sections may exceed 400 m ( D o d d e t al., 1988). However, it is unlikely that individuals could find their way through several kilometers of deep reservoirs and around dams. Successful movements through the lower reaches of Lost Creek to favorable habitats in other drainages are unlikely because they would require a move of > 15km to a dammed portion of Mulberry Fork, thence upstream another 25-30 km through the backwaters of Bankhead Lake. A straight-line overland movement of approximately 10kin to the north would put an individual in favorable habitat, but a railroad and several major roads would have to be crossed. Thus, flattened musk turtles in Lost Creek are almost certainly isolated from
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other populations, and there is probably no interchange between the three surviving populations, one of which is already small and shows no successful recruitment. This scenario is probably similar to that in other stream segments in the basin.
Threats to fragmented populations Once isolated, populations of S. depressus and other stream-dwelling turtles may be subject to a wide variety of natural and human-induced threats to their existence. In addition to the potential loss of genetic viability and heterozygosity in small fragmented populations, threats to S. depressus include: (1)
Small population size/abnormal population structure. Some flattened musk turtle populations (e.g. Gurley Creek) are composed of only a few large old individuals. In other populations, adults are common, but the absence of large juveniles or small adults (e.g. Turkey Creek) indicates no recent recruitment. Also, the sex ratio may be substantially skewed (Dodd, 1989). Because similar collecting methods and effort were used to sample all populations (Dodd et al., 1988), variation in population structure probably reflects the extent that various factors, including fragmentation, are affecting the population. Small populations are particularly vulnerable to both natural and human-caused perturbations. Even without direct external threats, such populations are vulnerable to stochastic events because of small size (Franklin, 1980; Soul6 & Simberloff, 1986; Pimm et al., 1988) and should be monitored closely.
(2) Disease. The largest population of S. depressus occurs upstream of Lewis Smith Lake in Sipsey Fork (Dodd et al., 1988). Presumably, this population is isolated from populations downstream by the reservoir. In 1985, a disease of unknown etiology struck this population, and the population declined by 50% within one season (Dodd, 1988). Although the population decline could not be solely attributed to disease, the vulnerability of small isolated igopulations to disease should be obvious. Turtles with disease symptoms have been observed in the Brushy Creek, and may be present in the downstream population in Lost Creek. (3)
Collecting. Easy access to collecting locations, docile disposition, attractiveness of individual turtles and rarity have combined to create a substantial demand for S. depressus before federal protection (US Fish and Wildlife Service, 1987). As many as 200 individuals may have been collected during July 1985 at Sipsey Fork (Dodd et al.,
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1988). Collectors also removed turtles in substantial numbers from other localities, and the lack of large adults in Blackwater Creek and of non-pitted small adults in Blackburn Fork is presumably the result of collecting pressure (Dodd et al., 1988).
CONCLUSIONS Through the process of stream capture (e.g. Lachner & Jenkins, 1971, for the fish Nocomis micropogon), geologic uplifts, glaciation and sea level fluctuations, natural fragmentation of drainage systems throughout the southeastern United States has led to repeated opportunities for colonization and speciation as streams were alternately connected and isolated. Barriers such as the Fall Line and the falls on the Kanawha River sometimes led to different faunas in upstream and downstream habitats or to the isolation of populations of widely ranging species (Tinkle, 1959; Jenkins et al., 1971; Hocutt et al., 1979; Seidel, 1981). As a result, there is a high degree of endemism and species richness for many taxa in drainages of the Southeast and Interior Low Plateau regions of the United States, particularly in rivers draining into the Gulf of Mexico (Ernst & Barbour, 1972; Branson, 1985; Fitzpatrick, 1986). Congeneric taxa often occupy adjacent drainages (e.g. the turtle genus Graptemys, Ernst & Barbour, 1972), and chromosomal and phenotypic differentiation often occurs among populations of a single species inhabiting adjacent drainages (Chambers, 1980, 1982; Bermingham & Avise, 1986). The habitat fragmentation occurring today is not related to change occurring in a geologic time scale. Instead, fragmentation results from direct modifications (e.g. channelization, dam construction, pulling snags used as aquatic turtle basking platforms) that in an ecological sense are instantaneous. Adverse modification of water quality also may be instantaneous (e.g. chemical spills), or may occur gradually over a longer time (e.g. siltation and sewage discharge). All contribute to the insularization of the diverse stream biota of southeastern North America. Adverse stream channel modification already has eliminated many mollusks (Stansbery, 1976; Stein, 1976) and fishes (e.g. Etnier et al., 1979), has altered native fish species composition (Timmons, 1982), and may be contributing to the decline of additional turtle species (US Fish and Wildlife Service, 1986). Sheldon (1988) suggested the importance of habitat fragmentation to stream faunas by presenting the analogy of rivers as archipelagos. In addition to being insular (i.e. between drainages), physical barriers on rivers, both natural and human-created, partition aquatic habitats into a series of
Turtle habitat fragmentation
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archipelagos. Although there is no way of knowing the extent of natural within-stream insularization for most taxa in aquatic habitats, humancreated fragmentation should force a reassessment of streams and rivers as contiguous habitats. The fragmentation of S. depressus habitat and the concomitant threats to its remaining populations dramatize the status of much of the freshwater stream biota throughout the southeastern and south-central United States. Immediate research needs to identify the microdistribution and status of this fauna, monitor changes in populations already known to be fragmented, and suggest ways to ameliorate both present and future deleterious effects of fragmentation. A C K N O W L E D G E M ENTS I thank Kevin Enge and James Stuart for field assistance. Bert Charest prepared Fig. 1. Robert Mount provided new information on Lost Creek turtles. Gary Meffe, Paul Opler and James D. Williams provided comments on various versions of the manuscript. Fieldwork was supported by a grant from the Office of Surface Mining, US Department of the Interior, and the Endangered Species Program, US Fish and Wildlife Service. These surveys were conducted under scientific collecting permits No. 172 and 259 from the Alabama Department of Conservation.
REFERENCES Bermingham, E. & Avise, J. C. (1986). Molecular zoogeography of freshwater fishes of the southeastern United States. Genetics, 113, 939-65. Branson, B. A. (1985). Aquatic distributional patterns in the Interior Lowland Plateau. Brimleyana, 11, 169-89. Chambers, S. M. (1980). Genetic divergence between populations of Goniobasis (Pleuroceridae) occupying different drainage systems. Malacologia, 20, 63-81. Chambers, S. M. (1982). Chromosomal evidence for parallel evolution of shell sculpture pattern in Goniobasis. Evolution, 36, 113-20. Dodd, C. K., Jr (1988). Disease and population declines in the flattened musk turtle Sternotherus depressus. Am. Midl. Nat., 119, 394-401. Dodd, C. K., Jr (1989). Secondary sex ratio variation among populations of the flattened musk turtle Sternotherus depressus. Copeia, 1989, 1041-5. Dodd, C. K., Jr, Enge, K. M. & Stuart, J. N. (1988). Aspects of the biology of the flattened musk turtle, Sternotherus depressus in northern Alabama. Bull. Florida St. Mus., Biol. Sci., 34, 1-64. Ernst, C. H. & Barbour, R. W. (1972). Turtles of the United States. University Press of Kentucky, Lexington. Etnier, D. A., Starnes, W. C. & Bauer, B. H. (1979). Whatever happened to the silvery
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minnow (Hybognathus nuchalis) in the Tennessee River? S.E. Fish. Counc. Proc., 2, 1-3. Fitzpatrick, J. F., Jr (1986). The pre-Pliocene Tennessee River and its bearing on crawfish distribution (Decapoda: Cambaridae). Brimleyana, 12, 123-46. Franklin, I. R. (1980). Evolutionary change in small populations. In Conservation Biology. An Evolutionary-Ecological Perspective, ed. M. E. Soul6 & B. A. Wilcox. Sinauer Associates, Inc., Sunderland, Massachusetts, pp. 135-49. Hocutt, C. H., Denoncourt, R. F. & Stauffer, J. R., Jr (1979). Fishes of the Gauley River, West Virginia. Brimleyana, 1, 47-80. Hubbs, C. L. & Miller, R. R. (1948). The zoological evidence: Correlation between fish distribution and hydrographic history in the desert basins of western United States. In The Great Basin, with Emphasis on Glacial and Postglacial Times. Bull. Univ. Utah, 38, 17-166. Iverson, J. B. (1977). Geographic variation in the musk turtle Sternotherus minor. Copeia, 1977, 502-17. Jackson, J. F. (1988). Crevice occupation by musk turtles: taxonomic distribution and crevice attributes. Anim. Behav., 36, 793-801. Jenkins, R. E., Lachner, E. A. & Schwartz, F. J. (1971). Fishes of the central Appalachian drainages: Their distribution and dispersal. In The Distributional History of the Biota of the Southern Appalachians, Part 111: Vertebrates, ed. P. C. Holt. VPI & State University, Blacksburg, Res. Div. Monogr. No. 4, 43-117. Kuehne, R. (1962). The classification of streams, illustrated by fish distribution in an eastern Kentucky creek. Ecology, 43, 608-14. Lachner, E. A. & Jenkins, R. E. (1971). Systematics, distribution and evolution of the chub genus Nocomis Girard (Pisces, Cyprinidae) of eastern United States, with descriptions of new species. Smithson. Contrib. Zool., 85, 1-97. Meffe, G. K. & Vrijenhoek, R. C. (1988). Conservation genetics in the management of desert fishes. Conserv. BioL, 2, 157-69. Mount, R. H. (1975). The Reptiles & Amphibians of Alabama. Agricultural Experiment Station, Auburn University, Auburn, Alabama. Ono, R. D., Williams, J. D. & Wagner, A. (1983). Vanishing Fishes of North America. Stone Wall Press, Washington, DC. Pimm, S. L., Jones, H. L. & Diamond, J. (1988). On the risk of extinction. Am. Nat., 132, 757-85. Seidel, M. E. (1981). A taxonomic analysis of pseudemyd turtles (Testudines: Emydidae) from the New River, and phenetic relationships in the subgenus Pseudemys. Brimleyana, 6, 25-44. Sheldon, A. L. (1988). Conservation of stream fishes: Patterns of diversity, rarity, and risk. Conserv. Biol., 2, 149-56. Shively, S. H. & Jackson, J. F. (1985). Factors limiting the upstream distribution of the Sabine map turtle. Am. Midl. Nat., 114, 292-303. Soltz, D. L. & Naiman, R. J. (1978). The natural history of native fishes in the Death Valley system. Nat. Hist. Mus. Los Angeles Cty, Sci. Ser., 30, 1-76. Soul6, M. E. & Simberloff, D. S. (1986). What do genetics and ecology tell us about the design of nature reserves? Biol. Conserv., 35, 19-40. Stansbery, D. H. (1976). Naiad mollusks. In Endangered and Threatened Plants and Animals of Alabama, ed. H. Boschung. Bull. Alabama Mus. Nat. Hist., 2, 42-52. Stein, C. B. (1976). Gastropods. In Endangered and Threatened Plants andAnimals of Alabama, ed. H. Boschung. Bull, Alabama Mus. Nat. Hist., 2, 21-41.
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Temple, S. A. & Cary, J. R. (1988). Modeling dynamics of habitat-interior bird populations in fragmented landscapes. Conserv. Biol., 2, 340-47. Timmons, T. J. (1982). Initial changes in fish species composition in two new lakes of the Tennessee-Tombigbee waterway, Alabama-Mississippi. S.E. Fish. Count. Proc., 4, 1-4. Tinkle, D. W. (1959). The relation of the Fall Line to the distribution and abundance of turtles. Copeia, 1959, 167 70. Tolson, J. S. (1984). Alabama coal data for 1983. Geol. Surv. Alabama, hTf~rmatioH Ser., 58E, Tuscaloosa, Alabama. US Fish and Wildlife Service (1986). Determination of threatened status tbr the ringed sawback turtle (Graptemys oculifera). Fed. Reg., 51, 45908 10. US Fish and Wildlife Service (1987). Determination of threatened status t~r the flattened musk turtle (Sternotherus depressus). Fed. Reg., 52, 22418-30. Wilcove, D. S., McLellan, C. H. & Dobson, A. P. (1986). Habitat fragmentation in the Temperate Zone. In Conservation Biology. The Science of Scarcity and Diversity, ed. M. E. Soul6. Sinauer Associates, Inc., Sunderland, Massachussetts, pp. 237-56. Wilcox, B. A. (1980). Insular ecology and conservation. In Conservation Bioloey. A n Evolutionary-Ecological Perspective, ed. M. E. Soul6 & B, A. Wilcox. Sinauer Associates, Inc., Sunderland, Massachusetts, pp. 95-117. Wilcox, B. A. & Murphy, D. D. (1985). Conservation strategy: the effects of fragmentation on extinction. Am. Nat., 125, 879 87. Whitcomb, R. F., Robbins, C. S., Lynch, J. F., Whitcomb, B. L., Klimkiewicz, M. K. & Bystrak, D. (1981). Effects of forest fragmentation on avifauna of the eastern deciduous forest. In Forest Island Dynamics in Man-Dominated Landscapes, ed. R. L. Burgess & D. M. Sharpe. Springer-Verlag, New York, pp. 125 292.