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    of 4
    90 Marsupial Frogs Fig. 7.21 Diversity of reproduction in hemiphractid frogs. A: eggs on the dorsum of Stefania ayangannae, from Mt. Kopinang, Guyana Cnote the blood vessels in the gill stalks and gills) 8: eggs developing in an open basin on the back of Frtziana goed from Rio de Janeiro, Brazil (note the two unfertilized eggs). C: embryos developing in a pouch with a middorsal sit-like opening in Flectonotus pyomaeus, fom Ocumare-de la Costa road, Aragua, Venezuela. D: direct develoament in a closed pouch of Gastrotheca Chistian, from Parque Nacional Calllegua, Jujuy, Argentina (note the protruding hatchling). Photos by D. B. Means (A), K.-H. Jungfer (B ané C), and M. Vaira (D), KUDA. the sperm and onto the back of the female—a new lineage was born, Hemiphractidae. The maintenance of this mode of reproduction led to other morpholog- ical, physiological, and behavioral adaptations that are unique to this lineage. The female, toting around a couple dozen eggs on her back, could easily loose some eggs. This problem, was solved by the production of a mucus layer on the back, to which the eggs could adhere. This mode of development exists to the present in members of the genera Cryptobatrachus, Hemiphractus, and Stefania (Fig. 7.214), Eggs that were naked on the female's back were, subject not only to desiccation, but also to predation by yolk-sucking wasps and flies. This dilemma was solved independently in three lineages. In the humid coastal forests of what is now southeastern Brazil, females developed dermal ridges on their backs, forming basin like structures that contained the eggs, which hatched before metamorphosis was completed (Fig, 7.21B). The advanced tadpoles survived in water-filled cavities in plants, Although they were capable of feeding, they could complete their metamorphosis by utilizing the yolk in their intestines, Meanwhile, far to the north in, what is now coastal Venezuela, another group of small frogs, the females of which were burdened by only a few large eggs developing in a pouch-like structure formed by longitudinal folds that met middorsally, deposited their advanced tadpoles in bromeliads (Pig, 7.21C), These tadpoles completed their metamorphosis solely by utilizing the yolk in their intestines, While these kinds of modification in the ftogs’ reproductive mode were going on, another important morphological change took place, In the most basal hemiphractids (Cryptobatrachus and Flectonotus), res piration was accomplished by a single pait of small gills. More effective respiration occurred through the development of a second pair of gills, which became far more extensive and eventually fused; these gills completely encased the embryo and yolk. Upon hatch ing, the gills were sloughed off as the froglet breathed by means of lungs. Egg transport and protection were further advanced by the formation of a permanent pouch on the back of the female in those taxa now recognized as marsupial frogs of the genus Gastrotheca, After the male exudes, sperm between the cloaca and the opening of the pouch, some eggs may roll from the uplified cloaca to the pouch; males learned to use their hind feet to move the eggs and direct them into the pouch. This was fa- cilitated by a dermal ridge leading to a large opening, in a pouch with @ median membrane. The pouch was not simply a pocket. Instead, immediately upon the entrance of eggs, membranous filaments containing, capillaries arose from the lining of the pouch, thereby ensuring a source of oxygen for each developing em- bryo. Upon hatching, the young could either simply crawl out of the pouch or be extruded, still possessing, their gills (Fig. 7.21D). Those that remained in the pouch were dug out by the female’s vigorous use of her feet. In western South America, crustal movements built cone of the most massive mountain ranges in the world, the Andes; for millions of years, the mountains rose higher and higher (chapter 8). On windward slopes of these mountains, the forests were continuously moist- ened by rain and dew from clouds, an ideal habitat for frogs of many kinds, including marsupial frogs. These latter frogs could spend their entire lives in the trees. Life in bromeliads was enhanced by brood pouches, that expanded laterally, so eggs developed on the flanks, of the female instead of on her back, thereby allowing, the frog to squeeze between the leaves. In one lineage, the pouches were lateral and then entered the body cavity, so eggs developed within the coelomic cavity. Some marsupial frogs ventured into the puna or paramo, treeless areas at high elevations, They lived on the ground but would crawl up small bushes at night; otherwise they maintained the life of a marsu. pial frog in the cloud forest, But one strain took on anew way of life; they retraced their evolutionary path and created more and smaller eggs that hatched as tadpoles, which were placed in ponds to undergo an exogenous development. These tadpole-producing marsupial frogs speciated in the high Andes; in some cases they reentered the cloud forests and returned to producing froglets instead of tadpoles, Reproductive Biology 91 ‘Thus hemiphractids took on a new way of repro- ducing. This was not a sole evolutionary event, but a series of correlated morphological and physiological changes that prompted behaviors unknown in any other frogs. These changes culminated in Gastrotheca, a genus truly deserving the name marsupial frogs. Gastrotheca is the only genus of frogs in which phylogenetic evidence points to reversals in the mode of their life history. The “re-evolution” of aquatic larvae within taxa having direct development is also known in the plethodontid salamander genus Desmog. nathus in eastern North America (Chippendale et al 2004; Chippindale and Wiens, 2005) and in the ances tral stock for three genera of indoryphlid caccilians in the Seychelles Islands (Mauro et al, 2014). In these cases, the evolutionary change is unidirectional, whereas some “re-evolved” lineages of Gastrotheca, there is a return to their ancestral state (chapter 3) LITERATURE CITED Alesla, A C. 1962, Breeding behavior and early development of | bogs of Negros, Philippine Islands. Copeia 1962:679-726. Altig, R, and G. F Johnston, 1989. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats, Herpetological Monogeaphs 3:81-108, Andersson, LG. 1911. A new Leptodactylus anda new Norotvema from Braail, Arkiv for Zoologi 7(17):1-6, Auber-Thomay, M., L. Coloma, and G. Onore. 1990. Blevage Sune rainetie marsupisle arhoricole des faréts nuageuses Equatoriennes, Gastrotbeca plumbea (Boulenger). Revue Frangaise d'Aquariologie, Herpétologie 17:57-62. Bahir, M_,M. Meogaskumbura, K. Manamendra-Arachchi, ©. Schneider, and R. 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Zeylanica 61-112, Brandes, G. and W, Schoenichen. 1901, Die Brutpflege der schwanziosen Bateachier,Abhandlungen dev Namax forschendien Gesellschaft zu Halle 22:395-481 92 Marsupfal Frogs Channing, A. 2001. Amphibians of Central and Souther Africa Ithaca, NY: Comstock, Chippindale, P.7., RM. Honett, A. S. Baldwin, and |. Wiens 2004, Phylogenetic evidence for a major reversal of life history evolution in plethodontid salamanders. Evolution 58-2809 2922, CChippindale, PT, and J.J. Wiens, 2005, Re-evolution of the larval stage in the plethodontid salamander Desmegnatls Herpetologieal Review 36:113-117 del Pino, B. M. 1980. Morphology of the pouch and incubatory integument in marsupial frogs. Copeia 1980:10-17. del Pino, E, M. 1996, The expression of Beachyury (T) during _gestrultion in the marsupial sto Gastotheca robambe. Developmental Biology 177:64-71. dll Bino, E, M., M. B. Avila, O. D. Pérez, M.S, Benitez, Alageén, ¥ Noboa, and I. M, Moya. 2004, Development of the dendrobatd frog Colostethus mackaiflla, International Journal of Developmental Biology 48663670 del Pino, B. M., and R. P Elinson, 1983, Gastrulation produces an embryonic dise, « novel developmentsl pattern for frags Nature 306:589-501, del Pino, E, M.,and B, Escobar. 1981, Embryonie stages of | Gastrotheea riobambae (Fowler) duriny maternal incubation and comparison of development with that of other egg: brooding hylid frogs. Journal of Morphology 167:277-295 dl Pino, B. M., M-L. Galarza, ©. M. de Abuja, and A. A. Hum phries J 1975. ‘The maternal pouch and development in the marsupial frog Gastosions nobambae (Fowler). Biological Bulletin 149:480-491 dlel Pino, E, M., and A. A. Humphries Jr 1878. Multiple nuclei uring carly oogenesis in Fectonotns pagmacus and other marsupial frogs: Biological Bulletin 154198-212, del Pino, &. M., M. Venegas Ferrin, A. Romero-Carvajal P, Montenegro-Lattes, N. Sienz-Ponce, |. M. Moya, I. Ala con, N. Sudou, S. Yamamoto, and M. Taira, 2007. A com- parative analysis of frog development. PNAS: Proceedings (of the National Academy of Sciences IDd: 11882-11888, Ducllman, WF, 1970, The hyd frogsof Middle America Monograph, Muscum of Natural History, University of Kansas 11-753, Ducllman, W.E,, and P. Gray. 1983, Developmental biology and systematics of the egg-brooding bylid frogs, genera Flectonotus and Fritziona. Herpetologiea 39:333-359, Ducliman, WE, K-H. jungfes, and D. C. Blackbusn. 201 ‘The phylogenetic relationship of geographically separated “Flectonotws” (Anura: Hlemiphtactidac), as revealed by molecular, behavioral, and morphological data, Phyllome- usa 10:25-29, Ducllman, W. E, and S, | Maness: 1980, ‘The reproductive behavior of some hylid marsupial frogs. Journal of Here: cology 14:213-222. Elinson, RP, and E. M. del Pino, 1985. Cleavage and gastru lation in the egg-brooding marsupial frog, Journal of Embryology and Experimental Morphology 90.225. 232, Eiinson, 8. 2, E. M. del Pino, D. S. Townsend, P. Eichhorn. 1990, A practical guide to the developmental biology of terrestrial breeding frogs Biological Bulletin 179: 163-177. Gadows, 1.1901, Amphibia and Reptiles. London: MacMillan, C. Cuesta, and Gagtiardo, R., B. Grifth, R. Hill, H. Ross, J. R. Mendelson II, E, Timpe, and B, Wilson. 2010, Observations on the captive reproduction of the horned marsupial frog Gastrthecs

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