EAR LOSS IN SKINKS APPENDIX 2 Material Examined The features of the middle ear were examined in the following specimens. Ablepharus grayanus: MCZ 84084; Acontias breviceps: MCZ 38559; A. g. gracilicauda: MCZ 100905; A. lineatus: MCZ 21416, 21659; A. meleagris: BMNH 63.2.21.21, MCZ 11934; A. percivali occidentalis: MCZ 67861, 67859; A. p. percivali: MCZ 40180; A. p. tasmani: MCZ 96905; A. plumbeus: AM R 76334, BMNH 94.6.29.38, MCZ 14233, 21452; Anomalopus gowi: AM R 63130; A. brevicollis: AM R 114084, QM 33853; A. leuckartii: AM R 43949; A. mackayi: AM R 13138; A. pluto: AM R 94362; A. swansoni: AM Palmer 5186, R 104139; A. verreauxii: AM R 6437 114043, MCZ 10263; Brachymeles bonitae: MCZ 20129; B. tridactylus: AM 98395; B. vermis: MCZ 26587; Calyptotis lepidorostrum: AM R 59246; C. scutirostrum: AM R 43061, 90434; Coeranoscincus frontalis: AM R 3823, QM J 45355; C. reticulatus: AM R 4795; Coggeria naufragus: QM J 59670; Davewakeum miriamae: FMNH 182546; Feylinia currori: AM R 97270, BMNH 1903.12.2.18, CAS 55112, MCZ 106990; F. elegans: MCZ 42886; ; F. grandisquamis: MNHN 1206.77; F. polylepis: MCZ 61215; Hemiergis decresiensis: AM R 93911, MCZ 49173, SAM 3237; H. initialis: MCZ 74976, WAM 13633; H. millewae: AM R 115996, SAM 3069B; H. per-
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onii; AM R 115711, MCZ 24595, 24648, 24652; H. quadrilineatum: MCZ 33210, WAM 35048; Isopachys anguinoides: AM R 112447; MCZ 74098; I. borealis: ZFMK 45714; I. gyldenstoplei: FMNH 178324; I. roulei: FMNH 196172, 196198, MCZ 74099; Larutia larutensis: BMNH 1946.8.3.19, MCZ 39265; L. sumatrensis: NHW 10172.1; Lipinia quadrivittatum: AMNH 86665, FMNH 152400; Melanoseps ater: subspecies: misukuensis: MCZ 50955; subspecies rondoensis: MCZ 52487; Menetia greyii: AM R 102024; M. surda: WAM 27981; Nannoscincus mariei: AM H 52097, R 125851, 146485, MCZ 92393; Nessia layardi: BMNH 1964.1720, MCZ 4122, unregistered; Ophiomorus brevipes: FMNH 141550; O. persicus: FMNH 141557; O. tridactylus: AMNH 75610, CAS 84679; O. raithmai: AMNH 85846; Ophioscincus cooloolensis: QM J 27381, 27384; O. ophioscincus: AM R 47642; O. truncatus: AM R 8666, 153851, 153868; Paracontias brocchi: MNHN 1979.8271; P. hildebrandti: MCZ 7767; P. holomelas: MNHN 7792; Saiphos equale: AM R 7242, 41197, AMNH 27266, MCZ 35344; Scelotes anguina: MCZ 131887; S. arenicolor: MCZ 14205; S. caffer: MCZ 131886; Scolecoseps boulengeri: MCZ 18357 (paratype); Typhlacontias brevipes: MCZ 96702; T. gracilis: AM R 76274, 76276; T. punctatissimus: TM 24471; T. rohani: FMNH 142787, 142791; Typhlosaurus caecus: AMNH 50669.
Journal of Herpetology, Vol. 36, No. 4, pp. 555–561, 2002 Copyright 2002 Society for the Study of Amphibians and Reptiles
Effect of Water Temperature and Oxygen Levels on the Diving Behavior of Two Freshwater Turtles: Rheodytes leukops and Emydura macquarii TONI E. PRIEST
AND
CRAIG E. FRANKLIN1
Department of Zoology and Entomology, University of Queensland, Brisbane, Queensland 4072, Australia ABSTRACT.—Rheodytes leukops is a bimodally respiring turtle that extracts oxygen from the water chiefly via two enlarged cloacal bursae that are lined with multi-branching papillae. The diving performance of R. leukops was compared to that of Emydura macquarii, a turtle with a limited ability to acquire aquatic oxygen. The diving performance of the turtles was compared under aquatic anoxia (0 mmHg), hypoxia (80 mmHg) and normoxia (155 mmHg) at 15, 23, and 308C. When averaged across all temperatures the dive duration of R. leukops more than doubled from 22.4 6 7.65 min under anoxia to 49.8 6 19.29 min under normoxic conditions. In contrast, aquatic oxygen level had no effect on the dive duration of E. macquarii. Dive times for both species were significantly longer at the cooler temperature, and the longest dive recorded for each species was 538 min and 166 min for R. leukops and E. macquarii, respectively. Both species displayed a pattern of many short dives punctuated by occasional long dives irrespective of temperature or oxygen regime. Rheodytes leukops, on average, spent significantly less time (42 6 2 sec) at the surface per surfacing event than did E. macquarii (106 6 20 sec); however, surface times for both species were not related to either water temperature or oxygen level.
Aquatic respiration is one of several strategies employed by freshwater turtles to extend dive 1 Corresponding Author. E-mail:
[email protected]. edu.au
duration (Belkin, 1968; Ultsch et al., 1984; Stone et al., 1992a). The capacity for aquatic respiration varies greatly among taxa, ranging from 4% of total oxygen uptake in the snapping turtle Chelydra serpentina (at 258C; Bagatto and Henry,
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1999a) to 37.5% in the softshell Apalone spiniferus (at 258C; Stone et al., 1992a). Although the degree of aquatic respiration has been quantified for many species and under many conditions, the implications of aquatic respiration on diving behavior remain unresolved. Two abiotic factors that affect diving behavior of bimodally breathing turtles are aquatic oxygen level and temperature (Ultsch, 1985). A positive correlation between aquatic oxygen level and dive duration has been consistently reported for the highly aquatic softshells (Ultsch et al., 1984; Ultsch, 1985; Stone et al., 1992b). Results for other taxa are less clear, with the moderately aquatic Chelydra serpentina (Ultsch et al., 1984), Chrysemys picta (Ultsch, 1985), and Sternotherus minor (Belkin, 1968) showing a positive relationship, whereas the moderately aquatic K. subrubrum (Stone et al., 1992b) does not. Temperature is an important confounding factor in studies of diving behavior of bimodally breathing turtles. Decreasing temperature resulted in an increase in the relative contribution of aquatic respiration in C. picta (Herbert and Jackson, 1985), Elseya latisternum (King and Heatwole, 1994b), and C. serpentina (Gatten, 1980). At lower temperatures, it may therefore be expected that the magnitude of the increase in diving time in response to increased partial pressures of oxygen (PO2) would be greater; that is, turtles would dive relatively longer in high PO2 water at low temperatures compared to low PO2 water. In support of this, S. odoratus displayed a positive relationship between PO2 and dive duration at 38C and 108C (Ultsch, 1985) but not at 238C (Stone et al., 1992b). In contrast, C. picta displayed a relationship at 108C (Ultsch et al., 1984; Ultsch, 1985) but not 38C (Ultsch and Jackson, 1982). In light of the contradictory results of the studies on the effects of aquatic PO2 and temperature on diving behavior, this study investigated the effect of temperature and PO2 on the diving behavior of two Australian pleurodires, Rheodytes leukops and Emydura macquarii, which vary in their capacity for aquatic respiration. Unlike the crypodires that obtain aquatic oxygen partly via the buccopharynx, pleurodires can obtain aquatic oxygen via enlarged cloacal bursae (King and Heatwole, 1994a). Cloacal respiration has reached its pinnacle in R. leukops, a chelid from northeast Australia. The cloacal bursae of this turtle are greatly enlarged and are lined with highly vascularized, multibranched papillae (Legler and Cann, 1980; Legler and Georges, 1993). By rhythmic ventilation of these structures, R. leukops is able to extract, on average, 41% of its oxygen requirements from the water (Priest, 1997; C. E. Franklin, M. Gordos, and T. Priest, unpubl. data). Emydura macquarii
does not have extensive cloacal modifications and has a limited capacity for aquatic respiration, extracting approximately 11% of its total oxygen consumption from the water (Legler and Georges, 1993; Priest, 1997). We hypothesize that diving time of both R. leukops and E. macquarii will be dependent on water temperature and that only R. leukops will respond to changes in aquatic oxygen level and that the degree of the response will be dependent on temperature. MATERIALS AND METHODS Six R. leukops (mean mass: 1325 g 6 193.9 SE; range: 595–1810 g) and five E. macquarii (mean mass: 1595 g 6 104.9 SE; range: 1200–1800 g) were used in this study. Emydura macquarii were collected from the Albert River, Brisbane and R. leukops from the Fitzroy R., Rockhampton, Queensland. Turtles were housed in two 2000liter covered outdoor holding tanks at 23 6 28C with water depth 250–300 mm. A full spectrum light was positioned above each tank, and a basking platform was provided, although R. leukops were never observed basking. Turtles were fed twice weekly with chopped meat and a variety of fruit and vegetables. The water was continually filtered and was changed after every feeding. Experiments were conducted at 158C, 238C, and 308C and at three aquatic PO2s: anoxia (0 mmHg), hypoxia (80 mmHg), and normoxia (155 mmHg), for each temperature. The temperatures chosen approximate the water temperatures over a year in the turtles’ natural home range. Turtles were placed in a rectangular tank (500 mm 3 1000 mm) that was filled to a depth of 250 mm with tap water and housed in a controlled temperature room. The water was continually circulated and filtered and the feeding regimen maintained. Rheodytes leukops were placed in the tank in pairs and E. macquarii in one pair and one group of three. Because the experimental tanks were relatively large and no interindividual aggression was observed, any effect of studying the turtles in groups rather than individually should be minimal. Turtles were marked with colored paint to allow individual recognition. Each group was allowed one week at 238C to become accustomed to the tank. Preliminary videotaping demonstrated that average dive time reached a plateau after this time. The temperature was then changed to the experimental temperature and the first PO2 level set. Temperatures were randomly selected, and then within each temperature the PO2 was again randomly selected. To minimize possible thermal stress to the animals, the test temperature was maintained until all three PO2 trials for that temperature had been completed. Maintaining
DIVING BEHAVIOR OF FRESHWATER TURTLES the test temperature until all PO2 treatments were completed may have allowed some thermal acclimation to occur; however, randomizing PO2 treatments and having multiple groups that were therefore presented with both temperature and PO2 in different order should remove any bias caused by possible thermal acclimation. To maintain the oxygen level a TPS dissolved O2 electrode (ED500) was suspended in the tank and connected to a TPS oxygen analyzer, model 2052A. The O2 analyzer was connected to a Mann Industries UTC/R Universal temperature alarm (thermocouple inputs) that was wired so that when the input from the oxygen analyzer moved beyond a preset level the alarm was tripped and a solenoid valve opened. The solenoid controlled the flow of either N2 or O2 through an airstone into the tank. The oxygen electrode was suspended at the outflow of the filter system to ensure a good flow of water over the electrode. The controlled temperature room was maintained on a 12:12 h light:dark photic regime. The duration of the trials was varied depending on the experimental temperature, being 24, 18, and 6 h for 15, 23 and 308C, respectively. The turtles had access to room air for the entire duration of the experiment, and basking platforms were not supplied. Experiments were videotaped during daylight hours only with a National F10 video camera and National AGG010 timelapse videocassette recorder. All tapes were later viewed and the emergence and submergence time of every dive during the experimental period was recorded. Statistical Analysis.—Dive time, surface time, and longest dive time were analyzed using a repeated measures three-way ANOVA. Analysis of dive and surface time was performed on the mean values for each turtle at each of the experimental conditions. When an effect was shown to be significant, differences among temperature, PO2, and species were detected using the least significant difference technique. Probability values less than 0.05 were taken as significant. Results are presented as means of treatments 6 SE, unless otherwise stated. RESULTS Dive Duration.—There was a significant difference in the way the species responded to changes in aquatic PO2 (F 5 6.51, P , 0.0025). Average dive time for R. leukops more than doubled from 22.4 6 7.65 min to 49.8 6 19.29 min when PO2 was increased from 0 to 155 mmHg (Fig. 1). In contrast, aquatic oxygen level had no effect on dive duration of E. macquarii (Fig. 1). Rheodytes leukops had on average significantly longer dives than E. macquarii in normoxic water
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FIG. 1. Average dive duration (min) of (A) Rheodytes leukops (N 5 6) and (B) Emydura macquarii (N 5 5) at 15, 23, and 308C under aquatic anoxia (0 mmHg), hypoxia (80 mmHg), and normoxia (155 mmHg). Bars are the mean of each treatment and error bars are 1 SE.
at all of the experimental temperatures (Figs. 1– 2). In hypoxic water, dives for R. leukops were significantly longer at 15 and 238C only. Under aquatic anoxia average dive duration of R. leukops and E. macquarii was not significantly different (Fig. 1) Decreasing temperature resulted in significantly longer dive durations for both species, but the magnitude of the response differed (F 5 10.03, P , 0.0001). Decreasing the temperature from 30 to 158C resulted in a sevenfold increase in dive time from 10.1 6 2.7 to 70.5 6 15.0 min in R. leukops and a fivefold increase in average dive duration from 6.7 6 1.2 to 31.3 6 8.3 min for E. macquarii. Average dive times of E. macquarii at 23 and 308C were not significantly different. The response to changes in PO2 shown by R. leukops was not dependent on temperature (F 5 1.87, P , 0.1256). Dive times under normoxia were approximately twice the length of dives under anoxia irrespective of temperature. Frequency of Dive Durations.—The longest dives recorded for R. leukops were at 158C and in normoxic water; the longest single dive recorded was 538 min. Although R. leukops was
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FIG. 2. Average maximum dive duration (min) of (A) Rheodytes leukops (N 5 6) and (B) Emydura macquarii (N 5 5) at 15, 23 and 308C under conditions of aquatic anoxia (0 mmHg), hypoxia (80 mmHg) and normoxia (155 mmHg). Bars are the mean of each treatment, error bars are 1 SE.
capable of extremely long dives, 41% of dives under the aforementioned conditions were less than 30 min (Fig. 3). For E. macquarii under equivalent conditions, the longest dive was 166 min, and 61.5% of dives were less than 30 min (Fig. 4). The extreme right skew of the dive time histograms was evident for both species and under all temperatures and aquatic oxygen levels (Fig. 3). Surfacing.—Surface times for both species were not significantly related to either water temperature or oxygen level (F 5 1.95, P . 0.15; Fig. 5). Rheodytes leukops, however, spent significantly less time at the surface after each dive than did E. macquarii, spending on average 42 6 2 sec at the surface between dives compared with 107 6 20 sec for E. macquarii (F 5 29.48, P , 0.0001). DISCUSSION Dive Duration.—Both aquatic oxygen level and temperature had a significant impact on the diving behavior of R. leukops, as would be expected based on previous studies of highly aquatic turtles. In contrast, the diving behavior of E. macquarii was influenced by water temperature only. Previous studies have demonstrated a cor-
FIG. 3. Frequency distributions of dive times for Rheodytes leukops (N 5 6) at 158C under aquatic anoxia, hypoxia, and normoxia. Observations for all individuals within a treatment have been combined. Bars are 15-min intervals.
relation between PO2 and dive duration in turtles with aquatic uptake capabilities similar to E. macquarii (Belkin, 1968; Ultsch et al., 1984; Ultsch, 1985); however, direct comparisons of the species in the different experiments are confounded by methodological differences. With the exception of the work of Stone et al. (1992) with A. spinifera, all these studies were conducted under forced submergence and generally concluded with the death of the turtles. Forced submergence leads to many physiological adjustments that are not seen in freely diving individuals. Such adjustments include a severe bradycardia and dramatically reduced metabolic rate (Belkin, 1964; Herbert and Jackson, 1985), increased anaerobic metabolism, and in some species increased aquatic respiration (Bagatto and Henry, 1999b). Studies with forcibly submerged animals may overestimate the relative contribution of aquatic respiration, and the turtles therefore may show a response that would not necessarily be present when diving freely. For example, S. odoratus under forced submergence displayed a correlation between aquatic PO2 and maximum dive duration but
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FIG. 4. Frequency distributions of dive times for Rheodytes leukops (N 5 6) and Emydura macquarii (N 5 5) at 15, 23, and 308C in normoxic water (155 mmHg). Observations for all individuals within a treatment have been combined. Bars are 15-min intervals.
did not show one under freely diving conditions (Ultsch et al., 1984; Stone et al., 1992b). It is therefore not surprising that under freely diving conditions only the highly aquatic R. leukops and not E. macquarii displayed a correlation between PO2 and dive duration. A correlation between temperature and dive duration is well documented in freshwater turtles (Fuster et al., 1997). The few studies that have examined the percent aquatic uptake at different temperatures have found that it increases at low temperatures (Gatten, 1980; Herbert and Jackson, 1985; King and Heatwole, 1994b). Accordingly dive times would be expected to be proportionally longer at low temperatures in high PO2 water compared to low PO2 water. Rheodytes leukops and E. macquarii, however, did not show such an interaction between temperature and PO2. Ultsch (1985), who studied A. spinifera, C. serpentina, and C. concinna and looked at survival time in relation to temperature and PO2, also observed no interaction, that is, the effect that increasing aquatic PO2 had on diving duration did not depend on temperature. The hypothesis that R. leukops uses its aquatic
respiratory ability to extend dive duration beyond that of E. macquarii is supported by this study. In anoxia, dive times of R. leukops and E. macquarii were approximately equal. In hypoxic water, dives of R. leukops were approximately twice as long as those of E. macquarii, and in normoxia the dives were three times longer, indicating the more oxygen that is available the more R. leukops is able to extend its dives beyond those of E. macquarii. This contrasts with the results of Stone et al. (1992b), who concluded that A. spinifera used their superior aquatic respiration to reduce the time spent at the surface rather than to increase dive duration beyond that of S. odoratus. These discrepancies may have been caused by differences in behavior and activity level between the species. Apalone spinifera in a later study had an aquatic O2 uptake of 21.7% (Bagatto and Henry, 1999b). In addition, S. odoratus may have become habituated to the experimental chamber, as normoxic trials were always conducted first. Bagatto and Henry (1999b) also found that dive times of A. spinifera in oxygenated water were twice as long as those originally recorded by Stone et al. (1992b).
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FIG. 5. Average time spent at the surface after each dive for both (A) Rheodytes leukops (N 5 6) and (B) Emydura macquarii (N 5 5) at 15, 23, and 308C and under conditions of aquatic anoxia (0 mmHg), hypoxia (80 mmHg), and normoxia (155 mmHg). Bars are the mean of each treatment, and error bars are 1 SE of the mean.
The relatively high proportion of short dives observed in this study is a common feature of studies with freshwater turtles (Stone et al., 1992b) and is supported by studies of oxygen use by diving turtles. These studies showed that after diving, turtles still had sufficient oxygen stores in their lungs and tissues to sustain continued respiration (Burggren and Shelton, 1979; Gatten, 1984; Burggren et al., 1989). In addition this pattern may be a result of different activity levels based on appetite and foraging or endogenous rhythms of daily activity levels. Surface Duration.—Surface duration was not related to either water temperature or oxygen content for either species, but R. leukops had significantly shorter surface times under all conditions. Rheodytes leukops is a highly aquatic turtle that spends the majority of its time on the river bed rather than in the water column (Legler and Cann, 1980). Emydura macquarii are less aquatic and are often observed engaged in both aerial and aquatic basking (Manning and Grigg, 1997). It is likely that E. macquarii would have spent time at the surface when not actually replenishing oxygen stores, whereas R. leukops remained at the surface only long enough to re-
plenish oxygen stores, as demonstrated by the fact that E. macquarii had much more variable surface periods than R. leukops. Stone (1992b) also demonstrated that A. spinifera, the species in their study that was most dependent on aquatic respiration, had the shortest and least variable surface period. At a given temperature, R. leukops dived longer than E. macquarii at high PO2, yet surface time was unrelated to PO2. The lack of correlation between dive and surface interval and the short surface interval suggests that the turtles were using aerobic metabolism. Ecological Implications.—Rheodytes leukops is commonly found in the riffle zones of its riverine habitat. These riffles are areas of relatively shallow, flowing water with a high level of saturated oxygen. Rheodytes leukops is a bottom dwelling turtle that forages on and among the rocks and debris of the substrate for aquatic invertebrates and algae (Legler and Cann, 1980; Cann, 1998). Cloacal respiration would therefore serve to greatly increase the amount of time the species can spend foraging and thus reduce the time and energy spent traveling to the surface. Emydura macquarii, in contrast, is a generalist and can be found in impoundments and large waterholes as well as riverine habitats. The benthic zone of deep waters are frequently anoxic, a habitat where cloacal respiration would be of no advantage. Acknowledgments.—This study was funded by a University of Queensland Foundation Grant and an Australian Research Council Grant to CEF. Financial assistance was also generously provided by Australian Geographic. All experimental procedures were approved by the University of Queensland animal ethics and experimentation committee (AEEC ZOO/375/96-00/ URG/H). Turtles were collected under Department of Environment Scientific Purposes permit C6/000064/96/SAA. LITERATURE CITED BAGATTO, B. P., AND R. P. HENRY. 1999a. Aerial and aquatic respiration in the snapping turtle, Chelydra serpentina. Journal of Herpetology 33:490–492. . 1999b. Exercise and forced submergence in the pond slider (Trachemys scripta) and softshell turtle (Apalone ferox): Influence on bimodal gas exchange, diving behavior and blood acid-base status. Journal of Experimental Biology 202:267–278. BELKIN, D. A. 1964. Variations in heart rate during voluntary diving in the turtle Pseudemys concinna. Copeia 1964:321–330. . 1968. Aquatic respiration and underwater survival of two freshwater turtle species. Respiration Physiology 4:1–14. BURGGREN, W. W., AND G. SHELTON. 1979. Gas exchange and transport during intermittent breath-
DIVING BEHAVIOR OF FRESHWATER TURTLES ing in chelonian reptiles. Journal of Experimental Biology 82:75–92. BURGGREN, W. W., A. SMITS, AND B. EVANS. 1989. Arterial oxygen homeostasis during diving in the turtle Chelodina longicollis. Physiological Zoology 62:668–686. CANN, J. 1998. Australian Freshwater Turtles. Beaumont Publishing Pte Ltd., Singapore. FUSTER, J. F., T. PAGES, AND L. PALACIOS. 1997. Effect of temperature on oxygen stores during aerobic diving in the freshwater turtle Mauremys caspica leprosa. Physiological Zoology 70:7–18. GATTEN, R. E. 1980. Aerial and aquatic oxygen uptake by freely-diving snapping turtles (Chelydra serpentina). Oecologia 46:266–271. . 1984. Aerobic and anaerobic metabolism of freely-diving loggerhead musk turtles (Sternotherus minor). Herpetologica 40:1–7. HERBERT, C. V., AND D. C. JACKSON. 1985. Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes, and cardiovascular function in aerated and anoxic water. Physiological Zoology 58:670–681. KING, P., AND H. HEATWOLE. 1994a. Non-pulmonary respiratory surfaces of the chelid turtle Elseya latisternum. Herpetologica 50:262–265. . 1994b. Partitioning of aquatic oxygen uptake among different respiratory surfaces in a freely diving pleurodian turtle, Elseya latisternum. Copeia 1994:802–806. LEGLER, J. M., AND J. CANN. 1980. A new genus and species of chelid turtle from Queensland, Australia. Contributions to the Scientific Natural History Museum of Los Angeles County 324:1–18. LEGLER, J. M., AND A. GEORGES. 1993. Family Chelidae, Chapter 21. In R. E. Jones (ed.), Fauna of Aus-
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tralia, Australian Government Printing Service, Canberra, Australian Capital Territory, Australia. MANNING, B., AND G. C. GRIGG. 1997. Basking is not of thermoregulatory significance in the ‘‘basking’’ freshwater turtle Emydura signata. Copeia 3:579– 584. PRIEST, T. E. 1997. Bimodal respiration and dive behaviour of the Fitzroy River turtle, Rheodytes leukops. Unpubl. honors thesis, University of Queensland, Brisbane, Queensland, Australia. STONE, P. A., J. L. DOBIE, AND R. P. HENRY. 1992a. Cutaneous surface area and bimodal respiration in soft-shelled (Trionyx spiniferus), stinkpot (Sternotherus odoratus), and mud turtles (Kinosternon subrubrum). Physiological Zoology 65:311–330. . 1992b. The effect of aquatic oxygen levels on diving and ventilatory behavior in soft-shelled (Trionyx spiniferus), stinkpot (Sternotherus odoratus), and mud turtles (Kinosternon subrubrum). Physiological Zoology 65:331–345. ULTSCH, G. R. 1985. The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 108C. Comparative Biochemistry and Physiology 81A:607–611. ULTSCH, G. R., AND D. C. JACKSON. 1982. Long-term submergence at 38C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water I. Survival, gas exchange and acid-base status. Journal of Experimental Biology 96:11–28. ULTSCH, G. R., C. V. HERBERT, AND D. C. JACKSON. 1984. The comparative physiology of diving in North American freshwater turtles. 1. Submergence tolerance, gas exchange and acid-base balance. Physiological Zoology 57:620–631. Accepted: 16 January 2002.
Journal of Herpetology, Vol. 36, No. 4, pp. 561–571, 2002 Copyright 2002 Society for the Study of Amphibians and Reptiles
A New Phrynobatrachus from the Upper Guinean Rain Forest, West Africa, Including a Description of a New Reproductive Mode for the Genus MARK-OLIVER RO¨DEL1
AND
RAFFAEL ERNST
Theodor-Boveri-Institute (Biocenter of the University), Department of Animal Ecology and Tropical Biology (Zoology III), Am Hubland, D-97074 Wu¨rzburg, Germany ABSTRACT.—We describe a new species of Phrynobatrachus from the Western part of the Upper Guinean rain forest, West Africa. Phrynobatrachus phyllophilus sp. nov. differs from all other known West African Phrynobatrachus by a combination of morphological and acoustical characters. It is most similar to Phrynobatrachus guineensis from which P. phyllophilus is distinguished by its almost white belly, presence of only one dark bar on femur and tibia, shape of the thumb in reproductive males, advertisement call, reproductive mode, and selection of different forest types. Phrynobatrachus phyllophilus is the first known species of the genus that deposits small clutches of eggs rich in yolk on leaves, in close vicinity to extremely small puddles on the forest floor. Its preferred habitats are swampy areas of primary rain forest. We also describe the tadpole of P. phyllophilus and the advertisement call of P. guineensis.
