CC BY-NC-ND 4.0 · Journal of Morphological Sciences 2018; 35(02): 142-152
DOI: 10.1055/s-0038-1669476
Original Article
Thieme Revinter Publicações Ltda Rio de Janeiro, Brazil

Morphological Alterations in the External Gills of Some Tadpoles in Response to pH

Caressa Maebha Thabah
1   Developmental Biology Laboratory, Department of Zoology, North-Eastern Hill University, Shillong, Meghalaya, India
,
Longjam Merinda Devi
1   Developmental Biology Laboratory, Department of Zoology, North-Eastern Hill University, Shillong, Meghalaya, India
,
Rupa Nylla Kynta Hooroo
1   Developmental Biology Laboratory, Department of Zoology, North-Eastern Hill University, Shillong, Meghalaya, India
,
Sudip Dey
2   Electron Microscope Laboratory, Sophisticated Analytical Instrument Facility, North-Eastern Hill University, Shillong, Meghalaya, India
› Author Affiliations
Further Information

Publication History

03 March 2017

03 August 2018

Publication Date:
31 August 2018 (online)

Abstract

Introduction Water pH affects the breeding, hatching, development, locomotion, mortality and habitat distributions of species in nature. The external gills of anuran tadpoles were studied by several authors in relation to abiotic factors. Exposure to low and high pH has been found to adversely affect the different tissues of various organisms. On that consideration, the present investigation was performed with tadpoles of the species Hyla annectans and Euphlyctis cyanophlyctis.

Material and Methods The maximum and the minimum pH thresholds were determined prior to the detailed experiments on the effects of pH. The pH that demonstrated 50% mortality was taken as the minimum and maximum pH thresholds. The hatchlings of both the species were then subjected to different pH (based on the minimum and maximum pH thresholds). After 48 hours of exposure, the external gills of the hatchlings were anesthetized and observed under a scanning electron microscope.

Results After 48 hours, clumping, overlapping and curling of the secondary filaments of the external gills and epithelial lesions in response to both acidic and alkaline pH were observed. The lengths of the secondary filaments were also affected by pH in both the species studied when compared with the control groups.

Conclusion Scanning electron microscopic approaches are relevant in assessing the adverse effects of pH on the morphology of the external gills of H. annectans and E. cyanophlyctis tadpoles, which included problems with osmoregulation, acid-base balance and respiratory function.

 
  • References

  • 1 Andren C, Henrikson L, Olsson M, Nelson G. Effects of pH and aluminium on embryonic and early larval stages of Swedish brown frogs Rana arvalis, R. temporaria and R. dalmatina. Holarct Ecol 1988; 11: 127-135
  • 2 Barth BJ, Wilson RS. Life in acid: interactive effects of pH and natural organic acids on growth, development and locomotor performance of larval striped marsh frogs (Limnodynastes peronii). J Exp Biol 2010; 213 (Pt 8): 1293-1300
  • 3 Schlichter LC. Low pH affects the fertilization and development of Rana pipiens eggs. Can J Zool 1981; 59: 1693-1699
  • 4 Pierce BA, Hoskins JB, Epstein E. Acid tolerance in Connecticut wood frogs (Rana Sylvatica). Herpetologia 1984; 18: 159-167
  • 5 Tome MA, Pough FH. . Responses of amphibians to acid precipitation. In T. A. Haines and R. E. Johnson, eds. Acid Rain/Fisheries. American Fisheries Society. , Bethesda, MD, 1982. , p. 245–254.
  • 6 Cummins CP. Effects of aluminium and low pH on growth and development in Rana temporaria tadpoles. Oecologia 1986; 69 (02) 248-252
  • 7 Dunson WA, Conell J. Specific inhibition of hatching in amphibian embryos by low pH. J Herpetol 1982; 16: 314-316
  • 8 Freda J, Dunson WA. The influence of external cation concentration on the hatching of amphibian embryos in water of low pH. Can J Zool 1985; a; 63: 2649-2656
  • 9 Freda J. and DUNSON, WA. Field and laboratory studies of ion balance and growth rates of Ranid tadpoles chronically - exposed to low pH. Copeia 1985; b; 2: 415-423
  • 10 Freda J, Dunson WA. Sodium balance of amphibian larvae exposed to low environmental pH. Physiol Zool 1984; 57: 435-443
  • 11 McDonald DG, Ozog JL, Simons BP. The influence of low pH environments on ion regulation in the larval stages of the anuran amphibian Rana clamitans. . Can J Zool 1984; 62: 2171-2177
  • 12 Dietz TH, Alvarado RH. Na and Cl transport across gill chamber epithelium of Rana catesbeiana tadpoles. Am J Physiol 1974; 226 (04) 764-770
  • 13 Brunelli E, Perrotta E, Tripepi S. Ultrastructure and development of the gills in Rana dalmatina (Amphibia, Anura). Zoomorphology 2004; 123: 203-211
  • 14 Nokhbatolfoghahai M, Downie JR. Amphibian hatching gland cells: pattern and distribution in anurans. Tissue Cell 2007; 39 (04) 225-240
  • 15 Gomez-Mestre I, Tejedo M, Ramayo E, Estepa J. Developmental alterations and osmoregulatory physiology of a larval anuran under osmotic stress. Physiol Biochem Zool 2004; 77 (02) 267-274
  • 16 Khan IA. . and KHAN AA. Physico-chemical conductions in Selkha Jheel at Aligarh. Journal of Environmental Ecology 1985; 3: 269-274
  • 17 Narayani N. . Seasonal changes in abiotic parameters of eutrophic wetlands (Lower Lake, Bhopal). In: Shula, A.C., Vandana, A. Trivedi, P.S. and Pandey, S.N. (Eds.), Advances in Environmental Biopollution. A.P. H. Publishing Corporation, New Delhi, 1990. , p. 155–163.
  • 18 Chaterjee G, Raziuddin M. Status of water body in relation to some physico-chemical parameters in Asansol Town, West Bengal. Proc Zool Soc India 2006; 5: 41-48
  • 19 Dutta SK. Amphibians of India and Sri Lanka (Checklist and Bibliography). , Odyssey Publishing House, Bhubaneswar, 1997. . p. 55 p.
  • 20 Chanda SK. Handbook of Indian Amphibians. : i–viii, Zoological Survey of India, Kolkata 2002. , p. 1–335.
  • 21 Molur S, Walker S. Amphibians of India Report Summary. Zoos Print. XIII 1998; 12: 1-29
  • 22 GOSNER. KL. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 1960; 16: 183-190
  • 23 Atland A, Barlaup BT. Rate of gastric evacuation in brown trout (Salmo trutta) in acidified and non-acidified water. Water Air Soil Pollut 1991; 60: 197-204
  • 24 Brunelli E, Tripepi S. Effects of Low pH acute exposure on survival and gill morphology in Triturus italicus larvae. J Exp Zoolog A Comp Exp Biol 2005; 303 (11) 946-957
  • 25 Dey S, Basu BT, Roy B, Dey D. A new rapid method of air-drying for scanning electron microscopy using tetramethylsilane. Journal of Microscopy (Oxford) 1989; 156: 259-261
  • 26 Freda J. and DUNSON, WA. Effects of low pH and other chemical variables on the local distribution of amphibians. Copeia 1986; 2: 454-466
  • 27 Gosner KL, Black IH. The effects of acidity on the development and hatching of New Jersey frogs. Ecology 1957; 38: 256-262
  • 28 Karns DR. . Toxic bog water in Northern Minnesota peatlands: ecological and evolutionary consequences for breeding amphibians [thesis]. University of Minnesota, Minneapolis, Minnesota, 1983
  • 29 Pough FH. Acid precipitation and embryonic mortality of spotted salamanders, Ambystoma maculatum. Science 1976; 192 (4234): 68-70
  • 30 Saber PA, Dunson WA. Toxicity of bog water to embryonic and larval anuran amphibians. J Exp Zool 1978; 204: 33-42
  • 31 Rowe CL, Sadinski WJ, Dunson WA. Effects of acute and chronic acidification on three larval amphibians that breed in temporary ponds. Arch Environ Contam Toxicol 1992; 23 (03) 339-350
  • 32 Pough FH. Wilson RE. Acid precipitation and reproductive success of Ambystoma salamanders. Water Air Soil Pollut 1977; 7: 307-316
  • 33 Heming TA, Blumhagen KA. Plasma acid-base and electrolyte status of rainbow trout exposed to alum (aluminum sulphate) in acidic and alkaline environments. Aquat Toxicol 1988; 12: 125-140
  • 34 Wilkie MP. , Wood CM. Recovery from high pH exposure in rainbow trout: white muscle ammonia storage, ammonia washout and the restoration of blood chemistry. Physiol Zool 1995; 68: 379-401
  • 35 Lin H, Randall DJ. The effect of varying water pH on the acidification of expired water in rainbow trout. J Exp Biol 1990; 149: 149-160
  • 36 Wright PA, Wood CM. An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environmental pH change and sodium uptake blockade. J Exp Biol 1985; 114: 329-353
  • 37 Brunelli E, Sperone E, Maisano M, Tripepi S. Morphology and Ultrastructure of the gills in two Urodela species: Salamandrina terdigitata and Triturus carnifex. Ita J Zool 2009; 76: 158-164
  • 38 Meyer EA, Cramp RL, Franklin CE. Damage to the gills and integument of Litoria fallax larvae (Amphibia: Anura) associated with ionoregulatory disturbance at low pH. Comp Biochem Physiol A Mol Integr Physiol 2010; 155 (02) 164-171
  • 39 Devi LM, Thabah CM, Hooroo RNK, Dey S. Scanning electron microscopic studies on the effect of pH on the gill morphology of Polypedates teraiensis hatchling (Amphibia: Anura). J Adv Microscop Res 2014; 9: 115-120
  • 40 Thabah CM, Devi LM, HOOROO RNK, DEY S. Microscopic studies on the effects of pH on the oral morphology of Hyla annectans tadpoles from North East India. J Adv Microscop Res 2014; 9 (04) 1-6
  • 40 Devi LM, Thabah CM, Hooroo RNK, Dey S. Morphological and microstructural changes of the oral apparatus in two Anuran tadpoles, in regard to pH. Micron 2016; 82: 41-51
  • 42 Daye PG, Garside ET. Histopathologic changes in surficial tissues of brook trout, Salvelinus fontinalis (Mitchill), exposed to acute and chronic levels of pH. Can J Zool 1976; 54 (12) 2140-2155
  • 43 Dey S, Kharbuli S. A transmission electron microscopical evaluation of environmental acid stress in a hill stream fish, Devario equipinnatus. National Academy Science Letters (India) 2010; 33: 5-6
  • 44 Freda J, Sanchez DA, Bergman HL. Shortening of branchial tight junctions in acid-exposed rainbow trout (Onchorhynchus mykiss). Can J Fish Aquat Sci 1991; 48: 2028-2033
  • 45 Laurent P, Perry SF. Environmental effects on fish gill morphology. Physiol Zool 1991; 64: 4-25
  • 46 McDonald DG. The effects of H+ on the gills of fresh water fish. Can J Zool 1983; 61: 691-703
  • 47 Prasad SK, Dey S, Singh OP. A scanning and transmission electron microscopic study on the effect of environmental acid stress on a hill stream fish (Brachydanio rerio) gill. J Adv Microscop Res 2011; 6: 255-262
  • 48 Rosseland BO, Staurnes M. . Physiological mechanisms for toxic effects and resistance to acid water: an ecophysiological and ecotoxicological approach. In: Steinberg, C.E.W Wright, R.F. (Eds.), Acidification of fresh water ecosystems: Implications for the future. John Wiley and sons, London, 1994. , p. 227–246.
  • 49 Ultsch GR, Bradford DF, Freda J. . Physiology: Coping with the environment. In: McDiarmid R.W., Altig. R (Eds.), Tadpoles: The Biology of Anuran larvae. University of Chicago Press, Chicago, 1999. , p. 189–214.
  • 50 Nokhbatolfoghahai M, Downie JR. The external gills of anuran amphibians: comparative morphology and ultrastructure. J Morphol 2008; 269 (10) 1197-1213
  • 51 Hossler FE, Rubey JR, Mcilwain TD. The gill arch of the mullet, Mugil cephalus I. surface ultrastructure. J Exp Zool 1979; 208: 379-397
  • 52 Hughes GM. Scanning electron microscopy of the respiratory surfaces of the trout gills. J Zool 1979; 187: 443-453
  • 53 Hughes GM, Umezawa S. Gill structure of the yellow tail and frog fish. J Ichthyol 1983; 30: 176-183
  • 54 Olsen KR, Fromm PO. A scanning electron microscopy study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z Zellforsch Microskopy Anatomy 1973; 143: 439-449
  • 55 Ojha J, Mishra AK, Munshi JSD. Interspecific variations in the surface ultrastructure of the gills of freshwater Mullets. Jpn J Ichthyol 1987; 33: 388-393
  • 56 Altig R, Mcdiarmid RW. . Body-plan development and morphology. In McDiarmid RW, Altig R (Eds.), Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, 1999. , p. 24–51
  • 57 Assheton HA. Notes on the ciliation of the ectoderm of the amphibian embryo. Q J Microsc Sci 1896; 38: 465-484
  • 58 Burggren W. Gas exchange, metabolism, and ventilation in gelatinous frog egg masses. Physiol Zool 1985; 58: 503-514
  • 59 Kessel RG, Beams HW, Shih CY. The origin, distribution and disappearance of surface cilia during embryonic development of Rana pipiens as revealed by scanning electron microscopy. Am J Anat 1974; 141 (03) 341-359
  • 60 Jagoae CH, Haines TA. Alterations in gill epithelium morphology of yearling Sunapee trout exposed to acute acid stress. Trans Am Fish Soc 1983; 112: 689-695
  • 61 Ramesh M. Effect of kitazin on the blood chemistry and histopathology of a freshwater fish Cyprinus carpio var. communis. Bharathiar University, Coimbatore, Tamilnadu, India. 1994 , p. 1–201.
  • 62 Neiboer E, Richardson RJ. The replacement of nondescript term heavy metals by a biologically and chemically significant classification of metal ions. Environ Pollut 1980; 1: 3-26
  • 63 Milligan CL, Wood CM. Disturbances in haematology, fluid volume distribution and circulatory function associated with low environmental pH in the rainbow trout (Salmo gairdneri). J Exp Biol 1982; 99: 397-415
  • 64 Evans DH, Piermarini PM, Choe KP. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 2005; 85 (01) 97-177
  • 65 Reid SD. . Adaptation to and effects of acid water on the fish gill. In: Hochachka, P.W. Mommsen, T.P. (Eds.), Biochemistry and Molecular Biology of fishes. Elsevier, New York, 1995. , vol. 5, p. 213–227.
  • 66 Bohmher J, Rahmann H. Influence of water acidification on amphibians. Fortschr Zool 1990; 38: 287-309