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Tennessee Cave Salamander Complex

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Tennessee Cave Salamander Complex Ecology and Natural History of Cave-dwelling Salamanders with an emphasis on the Tennessee Cave Salamander Complex Matthew L. Niemiller Department of Ecology and Evolutionary Biology March 27, 2007 Cave Colonization by Vertebrates • Limited by: – Darkness – Scarcity of Food – Dimension of Cavities • Classification: – Troglobite (Plethodontidae and Proteidae) – Troglophile (Ambystomatidae, Dicamptodontidae, Hynobiidae, Plethodontidae, Salamandridae) – Trogloxene – Accidental • 9 troglobitic salamanders – 8 in North America – All but 2 are paedomorphic • No sympatry Phenotypic Characters Associated with Cave-dwelling Salamanders Morphological Physiological Behavioral Reduced or Lost Eyes Metabolism Response to light Visual brain centers Circadian rhythms Aggression Pigmentation Fecundity Aggregation Body size Egg volume Metamorphosis Enlarged or Lengthened Chemo- and Life span Response to vibration mechanosensors Nonvisual brain centers Lipid storage Limbs Larval period 1 Cave-associated Traits Cave Development 2 Tennessee Cave Salamander Complex Gyrinophilus palleucus and G. gulolineatus • Aquatic troglobitic salamander • Endemic to subterranean waters of central and east TN, northern AL, and northwest GA • Little known about life history and ecology of the complex Warren County, TN 2004 (M Niemiller) Salamander Life Cycle 3 Pale Salamander Gyrinophilus palleucus palleucus Big Mouth Cave Salamander Gyrinophilus p. necturoides Berry Cave Salamander Gyrinophilus gulolineatus 4 Spring Salamander Gyrinophilus porphyriticus • Aquatic and terrestrial troglophile • Range from mountains of east TN to Cumberland Plateau • Larvae resemble G. palleucus in appearance but differ in eye size and head shape Cannon County, TN 2005 (B Miller) Spring Salamander Gyrinophilus porphyriticus Blue Ridge Spring Salamander Gyrinophilus porphyriticus danielsi 5 G. palleucus or G. porphyriticus? TN Cave Salamander adult Spring Salamander larva Rutherford Co., TN DeKalb Co., TN G. p. necturoides and the Stone Cave G. porphyriticus? Frick’s Cave, Walker Co. GA 6 Coffee Co., TN G. porphyriticus In Search of … The Tennessee Cave Salamander Processing TN Cave Salamanders 7 VI Alpha Tag Implanted TN Cave Salamander Distribution Central Basin Form G. gulolineatus G. p. necturoides G. p. palleucus Comparative numbers of Tennessee Cave Salamanders observed in selected historic sites from previous and the current study. Cave 1980s1 1990-91 Survey Current Study Franklin County Cave Cove Cave NA 32 (2 visits) 71 (2 visits) Custard Hollow Cave 10 0 (2 visits) 66 (2 visits) Lost Cove Cave 0 1 (1 visit) 0 (2 visits) Sinking Cove Cave NA NA 73 (3 visits) Grundy County Big Mouth Cave 8 6 (3 visits) 320 (12 visits) Knox County Cruze Cave NA 18 (2 visits) 368 (7 visits) Meade Quarry Cave NA NA 22 (2 visits) Mud Flats Cave 24 7 (2 visits) 15 (4 visits) Roane County Berry Cave 21 2 (2 visits) 5 (2 visits) Rutherford County Herring Cave 3 0 (1 visit) 12 (4 visits) Snail Shell Cave2 NA 0 (1 visit) 3 (2 visits) NA - Data not available 1 - Based on historic data from 1983-1989 in Caldwell and Copeland (1992) 2 - Snail Shell Cave system including Echo, Nanna, and Snail Shell Cave 8 SizeSize-Frequency-Frequency Histogram for G. p. palleucus and G. p. necturoides 14 n = 112 12 n = 131 10 8 G. p. palleucus 6 Frequency G. p. necturoides 4 2 0 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 SVL Size Class (mm) Size Class Information (in SVL) for Gyrinophilus palleucus Species 15-55 mm 56+ mm Total G. p. palleucus 14 (13%) 98 (87%) 112 G. p. necturoides 45 (34%) 86 (66%) 131 All Caves1 68 (25%) 201 (75%) 269 1 - except Cruze Cave and Meades Quarry Cave SizeSize-Frequency-Frequency Histogram for G. palleucus palleucus Localities 10 n = 22 9 n = 46 n = 44 8 7 6 5 Cave Cove Cave Sinking Cove Cave Frequency 4 Custard Hollow Cave 3 2 1 0 0 102030405060708090100 SVL Size Class (mm) 9 Size Comparison of Individuals > 70 mm SVL Between G. p. palleucus Caves 120.0 p = 0.00000016 100.0 p = 0.00000004 p = 0.000054 p = 0.000014 80.0 p = 0.0097 p = 0.0035 SV L ( mm) 60.0 Weight (g) 40.0 20.0 0.0 Cave Cove Cave Sinking Cove Cave Custard Hollow Cave Big Mouth Cave Population Size Time of Last Capture 1 2 3 4 5 6 29 Jun 2004 1 2 1 1 1 0 21 Jul 2004 2 8 9 1 2 06 Feb 2005 3 4 5 1 10 Mar 2005 4 6 2 17 Apr 2005 5 6 16 Jun 2005 6 Total marked (mtt)) 00 22 99 1414 1313 1111 Total unmarked (utt)) 66 2424 2222 1313 66 88 Total caught (ntt == mmtt ++ uutt)) 66 2626 3131 2727 1919 1919 Total released (stt)) 66 2626 3131 2727 1919 1919 Juveniles unmarked 4 2 3 6 6 6 •• ca. 365 m stream passage ••Jolly Jolly-Seber-Seber estimate of 97.1 individuals •• Schnabel estimate of 153.0 individuals Growth of Marked Individuals at Big Mouth Cave 100 L32 90 L30 L28 L14 L13 80 L09 L01 G97 L13 L32 70 L09 Snout-Vent Length (mm) Length Snout-Vent G97 L14 L28 L01 60 L30 50 0 50 100 150 200 250 300 350 400 Days 10 G. p. palleucus and G. p. necturoides Juveniles Franklin County, TN August 2004 Coffee County, TN October 2004 (M Niemiller) 24 mm SVL (M Niemiller) 26 mm SVL Potential Predation by Crayfish (Cambarus sp.) Roane County, TN, Mar. 2005 A B Other Predators? C D 11 Evolution of G. palleucus • G. palleucus at the western periphery of the range of G. porphyriticus • G. palleucus likely evolved from an epigean Gyrinophilus (Brandon 1971) • Low elevation populations of G. porphyriticus took refuge and became isolated in subterranean habitats during interglacial periods (Simmons 1975) Tennessee Cave Salamander Distribution mtDNA ML Phylogram Stereochilus marginatus Pseudotriton ruber G. porphyriticus A G. gulolineatusG. G. porphyriticusG. D G. palleucusG. G. porphyriticusG. B G. porphyriticus C G. G. porphyriticusG. danielsi BM1 ST1 MQ1 MF1 RR1 CR1 AS1 AN4 HC1 GF1 G1 GI1 MC1 SS1 B1 SR1 SA1 GS1 CC2 CH1 GA2 L1 P2 P3 GA1 PM1 CY1 SH1 WC3 WC1 CF1 S1 GPOR 1.00/ K2 1.00/ 1.00/ GI3 MU1 M2 C1 C2 F1 SM1 100 100 100 SP2 0.87/ 1.00/ 73 1.00/ 73 1.00/ 0.97/ 1.00/ 96 100 96 1.00/ 1.00/ 82 100 100 99 1.00/ 1.00/ 98 99 1.00/ 100 0.02 12 mtDNA Haplotype Distribution RAG-1 ML Phylogram G. porphyriticus NW GA, E TN CH4a,b, GA1a,b, MQ3b HC1b, HC2b G. porphyriticus NC SP2b 0.92 G. p. necturoides G2a,b, PG3a, WA1a, GI1a, GI3a BM10b 0.95 MC1a,b G. gulolineatus 0.89 G. p. palleucus B1a,b, B2a,b GS1a,b M1a MU3a EHR G. porphyriticus G1ab, M1b EHR G. porphyriticus SP1a,b Pseudotriton ruber Stereochilus marginatus 0.005 RAG-1 Haplotype Distribution 13 Divergence Among Major Clades G. palleucus G. gulolineatus ABCDE G. palleucus 0.1 - 0.9% G. gulolineatus 1.2 - 1.6% 0.1 - 0.4% A 1.4 - 2.5% 2.0 - 2.7% 0.1 - 2.1% B 2.2 - 2.4% 2.7 - 2.9% 2.1 - 2.9% 0.0 - 0.0% C 2.8 - 3.1% 2.9 - 3.1% 2.8 - 3.5% 3.2 - 3.4% 0.9 - 0.9% D 3.4 - 4.0% 3.8 - 4.3% 3.6 - 4.5% 3.8 - 4.2% 3.4 - 3.9% 0.1 - 2.2% E 4.7 - 4.9% 4.8 - 5.1% 4.7 - 5.3% 5.0 - 5.0% 4.8 - 4.9% 4.8 - 5.0% NA G. palleucus G. gulolineatus ABCDE G. palleucus 0.05 - 1.80 Myr G. gulolineatus 0.60 - 3.20 Myr 0.05 - 0.80 Myr A 0.70 - 5.00 Myr 1.00 - 5.40 Myr 0.05 - 4.20 Myr B 1.10 - 4.80 Myr 1.35 - 5.80 Myr 1.05 - 5.80 Myr 0.00 - 0.00 Myr C 1.40 - 6.20 Myr 1.45 - 6.20 Myr 1.40 - 7.00 Myr 1.60 - 6.80 Myr 0.45 - 1.80 Myr D 1.70 - 8.00 Myr 1.90 - 8.60 Myr 1.80 - 9.00 Myr 1.90 - 8.40 Myr 1.70 - 7.80 Myr 0.05 - 4.40 Myr E 2.35 - 9.80 Myr 2.40 - 10.20 Myr 2.35 - 10.60 Myr 2.50 - 10.00 Myr 2.40 - 9.80 Myr 2.40 - 10.00 Myr NA Cruze Cave Meade Quarry Cave Gyrinophilus sp. 14 TAG Amphibian Cave Survey • 122 caves, 213 surveys • Amphibians: 14 salamanders (2818 records), 10 frogs (312 records) • Reptiles: 3 snakes (5 records), 1 lizard (1 record), 1 turtle (3 records) Sampling Localities 15 Cave Amphibian Records Salamanders Frogs Gyrinophilus gulolineatus (44, TB) Rana palustris (173, TX) Gyrinophilus palleucus (676, TB) Rana clamitans (100, TX) Gyrinophilus porphyriticus (436, TP) Rana catesbeiana (32, TX) Eurycea lucifuga (851, TP) Rana sphenocephala (1, AC) Eurycea longicauda (78, TP) Bufo americanus (1, AC) Eurycea cirrigera (66, TX) Bufo fowleri (1, AC) Pseudotriton ruber (225, TP) Gastrophryne carolinensis (1, AC) Plethodon dorsalis (62, TX) Pseudacris crucifer (1, AC) Plethodon glutinosus (340, TX) Hyla chrysoscelis (1, AC) Plethodon petraeus (4, TX) Acris crepitans (1, AC) Desmognathus abditus (1, AC) Desmognathus conanti (33, TX/AC) Hemidactylium scutatum (1, AC) Notophthalmus viridescens (1, AC) Cave Reptile Records Squamates Turtles Crotalus horridus Terrapene carolina (3 records) Elaphe obsoleta (3 records) Nerodia sipedon Scincella lateralis Spring Salamander Gyrinophilus porphyriticus • 438 records • 14 caves • Adults and larvae • Cannibalism • Parasites 16 Southern Two-lined Salamander Eurycea cirrigera • 66 records • 8 caves • Adults, larvae, and eggs •Migration • Oviposition Eurycea cirrigera Egg Development Eurycea cirrigera Egg Development Egg Mass Distance from Mass Surface Area 26 Jan 09 Feb 26 Feb Entrance (m) (mm2) 1 46 1408 61 (11)1 61 (31)1 60 (42) 2 53 1440 56 (26)1 53 (40)1 HT 3 56 1400 58 (29) 4 59 1443 32 (37) 31 (43) HT 5 64 986 61 (10) 46 (29) HT 6 38 1426 54 (38) HT HT 7 91 1080 65 (19) 8 38 2183 71 (21)1 9 61 1512 38 (38) 1Adult female found in attendance of egg mass.
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