Available online at http://www.ifgdg.org

Int. J. Biol. Chem. Sci. 12(3): 1484-1493, June 2018

ISSN 1997-342X (Online), ISSN 1991-8631 (Print)

Review Paper http://ajol.info/index.php/ijbcs http://indexmedicus.afro.who.int

Bibliographic synthesis on biology and ecology of Hoplobatrachus occipitalis (Günther, 1858)

Théophile GODOME1,2*, Ephrem TOSSAVI1, Nahoua Issa OUATTARA2 and Emile Didier FIOGBE1,2

1Laboratory of Research on Wetlands, Department of Zoology, Faculty of Sciences and Techniques, University of Abomey-Calavi, BP: 526 Cotonou, Benin. 2Laboratory of Hydrobiology, UFR Biosciences, University Félix Houphouet-Boigny, 22 BP: 582 Abidjan 22, Côte d’Ivoire. *Corresponding author; E-mail: [email protected]; Tel: (+229) 95 64 65 17

ACKNOWLEGMENTS The authors thank World Bank through African Center of Excellence on Climate, Biodiversity and Sustainable Agriculture (CEA-CCBAD) for financial support.

ABSTRACT

Hoplobatrachus occipitalis is a frog belonging to Dicroglossidae family, the most spread in West Africa. This study aimed at performing to bibliographic synthesis on biology and ecology of this species in order to assess its potential in aquaculture. It lives along banks, rocky reservoirs and earthen ponds and prefers savannah areas. It feeds on coleopterans, caterpillars, spiders, vegetal fragments, fishes, crabs, ants, grasshoppers, locusts, dragonflies, frogs, mollusks, lizards, mice, butterflies, wasps and diptera larvae. The growth of H. occipitalis depend on the temperature and pH of the medium. A pH range 6.2 and 7 and temperature equal or upper, than 28 °C are suitable for its growth. H. occipitalis is an oviparous species. Its first sexual maturity height is 124.5 mm for females and 95 mm for males and it often reproduces during rainy season. The rapid growth, resistance and high nutritional quality of this species are some of its important potentialities for aquaculture. Natural reserves of H. occipitalis are overexploited and therefore no more able to satisfy the populations demand. A successful breeding of this species can help not only to preserve and strengthen the natural reserves but to produce regularly bulbous crowfoot for human consumption. © 2018 International Formulae Group. All rights reserved.

Keywords: Hoplobatrachus occipitalis, biology, ecology, aquaculture potentialities.

INTRODUCTION tritons and salamanders) and others (FAO, Worldwide fresh water aquaculture 2016). production reaches 47.1 million tons during In Africa, continental aquaculture 2015 owing to the rapid development of produces 1.7 million tons during 2015 and is rearing technique of certain species such as made of fishes, mollusks, crustacea and other Nile Tilapia (Oreochromis niloticus), Clarias aquatic animals including frog (FAO, 2016). gariepinus, some amphibians (frog, toad, Frog is an amphibian that may be naturally found in tropical and subtropical

© 2018 International Formulae Group. All rights reserved. 6033-IJBCS DOI: https://dx.doi.org/10.4314/ijbcs.v12i3.33 T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018 climate regions. Like every amphibian, it is a from 0.7 to 0.9 mm; several dorsal warts poïkilotherm animal. Likewise, its growth is arranged longitudinally and a minuscule directly tied to the temperature. Another internal metatarsal tubercle. It has a complete characteristic is the double respiratory system, strap between fingers and toes; a very either pulmonary or cutaneous (Morin, 2008). verrucose skin though eyes and nostrils are Ecologically, these animals play an dorsally positioned. The skin is very slippery important role in food web and are due to numerous glands. Mussel-anal length indispensable to wetlands balance maintaining of adult males varies from 52 to 104 mm and (Channing, 2001). Frogs are excellent bio- that of the biggest females measured in the indicators of aquatic environment (Schiøtz, national zoo area of Comoé was 65 mm. 1999; Rödel, 2000; Channing, 2001; Guerry According to Loveridge (1955), mature and Hunter, 2002). Indeed, they consume female of H. occipitalis can weight 235 g with harmful insects reducing therefore their a mussel-anal length about 127 mm. However, population. By doing so, they enhance Perret (1966) reported mussel-anal length agricultural production and contribute to the varies from 52 to 110 mm in males and 110 to fight against malaria vectors (Channing, 135 mm in females. Males weight varies from 2001). 24 to 84 g and while females weigh from 20 Economically, some edible frog to 132 g (Rödel, 2000). H. occipitalis species like Hoplobatrachus occipitalis specimens individuals have a large mouth. constitute a source of animal genuine proteins The side of inferior jaw carries three teeth. and income to men (Neveu, 2004; They pupil are oval and vertical. The eardrum Nzigidahera, 2006). is distinct and bordered by a bent supra- Several studies inform on the diet tympanic fold. Males have pairs of lateral (Alfredo, 1996; Mady-Goma, 2012), the vocal sack and large thenar tubercle; the skin biology (Wells, 1977; Barbault, 1984; Heyer surrounding vocal sacks in the throat is et al., 1994; Rödel, 2000; Morin, 2008; Tohé, strongly folded. Posterior members are 2009), the ecology (Rödel, 2000 ; Wildlife et relatively short and muscled than anterior al., 2007; Tohé, 2009), the parasitology members. Stems are generally longer than (Akani et al., 2011; Aisien et al., 2014) and thighs. There are many small tubercles on the the sensitivity to heavy metals (James and posterior part of thighs (Rödel, 2000). Little, 2003 ; Ezemonye and Enuneku 2005; The body color of H. occipitalis is Sobha et al., 2007; Ezemonye and Enuneku, green-yellowish, olive or brown-dull; its back 2011; Idowu et al., 2014; Omonona et al., presents greenish or blackish spots which 2016) of H. occipitalis, but studies regarding sometimes form lines. Black spots are also frogs rearing especially H. occipitalis from present on the superior lip; most of individuals larval stage to adult are scarce in West Africa. have their throat and inferior lip white colored Besides, data on the feeding habit of this frog with rarely some black spots. The external species are very important for the parts of thighs are marbled. The belly is white qualification of its growth performance and with sometimes some black spots (Rödel, production cost reduction. H. occipitalis 2000); vocal sacks are grey, bluish (Burton, rearing in controlled medium can help 1972) or cream colored (Loveridge, 1955). promoting these species. In order to preserve and strengthen the natural stock. The rearing SYSTEMATICAL POSITION OF achievement of this frog species requires HOPLOBATRACHUS OCCIPITALIS knowledge on its biology, ecology and The species name has progressed as a aquaculture potential. This article summarizes function of time. Indeed, Rana occipitalis some studies on H. occipitalis. (Scortecci, 1936), Rana tigrina occipitalis (Dekeyser and Villiers, 1956), MORPHOLOGY DESCRIPTION OF H. Hoplobatrachus occipitalis (Dubois, 1992) are OCCIPITALIS synonym to Hoplobatrachus occipitalis H. occipitalis is a large and flat ranidae (Günther, 1859). According to Frost et al. with globular eyes which diameter ranges, (2006), Hoplobatrachus occipitalis belongs to 1485

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Regnum of Animalia; Phyllum of Chordata; (Rödel, 2000; Wildlife et al., 2007). Its natural Sub-phyllum of Vertebrata; Class of habitats are thus sub-tropical forests, dry Amphibia; Sub-class of Lissamphibia; Super- savannah, wet savannah, tropical or sub- order of Salienta; Order of Anura; Familia of tropical prairie of dry plains, tropical or sub- Dicroglossidae; Sub-familia of Dicroglossinae tropical prairie of periodically flooded plain, and Genus Hoplobatrachus. rivers and intermittent rivers, fresh water lakes and intermittent fresh water lakes, fresh water GEOGRAPHICAL DISTRIBUTION swamp and intermittent fresh water swamp, Hoplobatrachus occipitalis fresh water sources, tillable grounds, pastures, distribution is mainly disjunctive including the rural gardens and ponds (Rödel, 2000). Northern Africa (Morocco, Algeria and According to Alfredo (1996), in Libya) stock and a great part from sub- Northern Africa, H. occipitalis dwells in oasis, Saharan Africa. These populations can still be in mountain regions where it lives in wells considered isolate with sub-populations in the and cisterns. It is active the day and inactive at South-West of Libyan Jamahiriya Arab, night and during the winter. South-East of occidental Sahara and close to Besides, the life cycle of frogs includes Mauritania, Mountains area of Niger and the two distinct stages: aquatic stage and Northern Mali. In sub-Saharan Africa, it is terrestrial stage. The last one requires found on the Atlantic coast by the East, in consumption of high proteins value feed for Ethiopia, Chad, Sudan and Southern Angola their growth (Olvera-Novoa et al., 2007). and Mozambique. Other sub-Saharan African Nevertheless, they have a rapid growth countries such as Northern Zambia, Western in hot climates and low in temperate climates Congo, Senegal, Gambia, Bissau Guinea, due to their poïkilotherm characteristic. Liberia, Sierra Leone, Guinea, Mali, Burkina Therefore, they hibernate and their activity is Faso, Ivory Coast, Ghana, Togo, Benin, limited to the mid of year in temperate climate Niger, Nigeria, Cameroon, Equatorial Guinea (Morin, 2008). Especially, temperature is (including Fernando Pó isle), Congo, important for the growth of H. occipitalis Democratic Republic of Congo, Republic of since values upper than 28 °C enable its Centrafrica, Uganda, Kenya, Tanzania, normal growth but at values lower than 25 °C, Rwanda and Burundi (Rödel, 2000). Research the growth is slowed down. Furthermore, a pH carried out by Frost (1985) confirm the ranged between 6.2 and 7 does not influence existence of H. occipitalis in the area of the growth of H. occipitalis (Nzigidahera, Senegal to Ethiopia, from Northern to 2006). It is important to notice that a period of Southern Zambia, Angola and Southern two years is necessary for them to reach Congo. According to Alfredo (1996), H. sexual maturity and more for commercial occipitalis is an Ethiopian species recorded in height (Morin, 2008). the North-West Africa, South-West Libya, Adrar Iforas (Mali), Adrar (Mauritania) and FOOD HABIT the rocky areas of Niger. Generally, frogs are recognized like electrical diet animals (Perret, 1966). They are ECOLOGY live prey predators. H. occipitalis essentially H. occipitalis inhabits along river feeds on coleopterans, caterpillars, spiders, banks, rocky reservoirs and earthen ponds vegetal fragment, fishes, crabs, ants, with a preference to savannah environments. grasshoppers, locusts, dragonflies, frogs, This species may be found in some woody mollusks, lizards, mice, butterflies, wasps area (Poynton and Broadley, 1985) and in an (Mady-Goma, 2012). According to Alfredo eco-region with both savannah and forest: that (1996), it feeds on coleopterans, orthopterans, is the case of Miombo forest of central toads (de Xeros Bufo) and their tadpoles and Zambia (Gruschwitz et al., 1991). It also individuals from their own species. Rödel dwells into rocky reservoirs of rivers (2000) reported that H. occipitalis larvae are surrounding by primary forest where high carnivorous though preys are larvae from water temperature (until 40 °C) is recorded other frog species, mosquito larvae and other 1486

T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018 aquatic species larvae. An observation of their environmental conditions (photoperiod, stomach content showed Coleopterans, temperature, precipitations, humidity) (Kühn Diptera, Lepidoptera, Hymenoptera, et al., 1987). This is especially favoured in Orthopterans, mollusks, soft substances and ponds near rivers filled up by the firs rain (van vegetal fragments (Nzigidahera, 2006). den Elzen and Kreulen, 1979). Thus males Lescure (1971) showed that H. occipitalis diet floating at water surface attract females by includes essentially Coleopterans, spiders and their croaking. Spawn often happens in the Orthopterans. These predators select their water and eggs quantity may range between prey according to its speed, movement and 800 and 1500 (Barbault, 1984; Rödel, 2000). size. The important proportion of Eggs are laid individually or in small Coleopterans in the frog diet indicates its group forming sticking frost on rocks or ability to live nearby rivers (Inger and Marx, stones at the water bottom. The sticking frosts 1961; Rödel, 1995). Observations made by are covered by algae and detritus making eggs Loveridge (1942) showed H. occipitalis feeds are less visible. Eggs diameter averages 5 mm on other frog species. Also, Noble (1924) at pharyngula stage and 3.2 mm at neurula reported this frog feeds on its fellows. stage (Rödel, 2000). According to Tohé et al. According to Kühn et al. (1987), all ranidae, (2016), mature eggs size is 2.74 mm. insects and fishes are considered as prey of H. A study led by Zug (1987), show eggs occipitalis which lives in water during the measured 1.6 mm to 1.8 mm and possess day. It leaves the water for hunting at night black and white poles. Parker (1936) but in full moon period it stays in water. In described clutch as a huge floating egg mass. Northern Africa, H. occipitalis is active in the However, these authors have made confusion day and at night but inactive during the winter between Hoplobatrachus occipitalis eggs and (Alfredo, 1996). Spieler and Linsenmair those from other species (probably (1998) confirmed this species is active at night Phrynomantis microps). and stay hidden from the sun rise to sunset. Moreover, food conditions of frog are PARASITE FAUNA OF not well defined. Carnivorous fish rations are HOPLOBATRACHUS OCCIPITALIS used in frog rearing farm (Casali et al., 2005). Parasites are the most recorded pathogens in aquaculture. Parasitological REPRODUCTION studies are so very important for the Reproduction is an important factor to development of fish breeding potential in the success of intensive production of animal. fresh water habitats. Some studies showed Moreover, frogs reproduce only during hot Hoplobatrachus occipitalis may be infested in temperature period. In temperate climates, different organs by several parasites (Table 1). frogs reproduce only during the summer (Morin, 2008). HEMATOLOGY AND SENSITIVITY TO However, the reproduction of H. HEAVY METALS occipitalis occurs in the rainy season under Cadmium is a heavy metal without any sub-tropical climate (Rödel, 2000). Males are biological function. It is very toxic to both small and possess vocal sacks which are aquatic and terrestrial organisms. It was powerful resonator (Perret, 1966). The first introduced in aquatic environment mainly by maturity height is 124.5 mm for females and human activities including mine exploitation, 95 mm for males (Tohé et al., 2016). The least fertilizers using and industrial discharges height of first maturity for females is 122 mm (Volgiatzis and Loumbourdis, 1997; James and 68 mm for males. All individuals reach and Little, 2003; Ezemonye and Enuneku, sexual maturity at 130 mm for females and 2005). Adult frogs can absorb cadmium by 120 mm for males (Tohé et al., 2016). Their skin or by oral way by consuming water and croaking is especially tied in reproduction by respiration (Ezemonye and Enuneku, (Wells, 1977; Heyer et al., 1994). Females of 2011). Then, it can pass through many tissues H. occipitalis show an annual variation in particularly liver, kidneys, gonads, placenta, their reproduction capacity even in constant 1487

T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018 brain, bones and blood (Sobha et al., 2007; source of income. For instance, peasants sell Omonona et al., 2016). edible frogs Hoplobatrachus and Ptychadena Furthermore H. occipitalis accumulates to big hotels and restaurants in Bujumbura highly zinc, following successively by iron, (Nzigidahera, 2006). Therefore, H. occipitalis copper, Nickel and lead (Idowu et al., 2014). is the most sold because it is easy to harvest and has a big thigh with an important PROSPECTIVE FOR AQUACULTURE economical value. Frogs constitute an important animal A survey made by “Fondation Droit proteins source in Africa (Onadeko et al., Animal”, Sciences and Ethic (LFDA) during 2011). Populations of Nigeria, Côte d’Ivoire, the first months of years 2008 and 2009 in Benin and Burkina Faso include increasingly three countries (Nigeria, Benin and Burkina frog meat in their menu: either grilled or Faso) by questioning villagers, commercials, boiled. Fishermen obtained 20 dollars for a hunters, dealers and customer-consumers thousand of dried frog. Most of them were showed that among the 25 species considered, adapted to this activity because it is more H. occipitalis is the most consumed in both profitable than fish (DDC, 2010). The extent Burkina Faso and Nigeria following by of this activity constitutes a threat to Pyxicephalus edulis, Ptychadena bibroni, ecosystems. H. occipitalis is more appreciated Ptychadena oxyrynchus and Ptychadena by consumers but its tadpoles are useful trinodis (LFDA, 2011). Frogs sale concerns because for example, they consume mosquito mainly human consumption. However, certain larvae (DDC, 2010). Biologist required frogs species are used in traditional medicine, rearing farm in order to preserve wild especially toads or frogs resembling to toads populations (DDC, 2010). (LFDA, 2011). According to Nzigidahera (2006), exploitation of edible frogs constitutes a

Figure 1: Specimen of Hoplobatrachus occipitalis (Günther, 1858).

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 Residence zone of the species

Figure 2: Distribution of Hoplobatraclius occipitalis in Africa (Cartographical Data©2017 Google. INEGI).

Table 1: Parasites of Hoplobatrachus occipitalis and infested organs.

Parasites (Species) Phylum Organs

Microfilariae Folleyellides sp (Aisien et al., 2014) Nematoda Blood

Aplectana acuminata (Akani et al., 2011) Nematoda Bowel

Oxyuris sp. (Akani et al., 2011) Nematoda Bowel and Colon

Eurytrema sp. (Akani et al., 2011) Nematoda Stomach, Bowel and colon

Diphyllobothrium sp. (Akani et al., 2011) Cestoda Bowel

Eimeria terraepokotorum (Miloslav et al., 2006) coccida Bowel

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CONCLUSION 2005. Avaliação de rações comerciais In summary, we can say that H. nas fases de crescimento e terminação da occipitalis is a very robust species that recria de rã-touro. Boletim do Instituto de deserves to be reared because it is an Pesca, 31(1): 37-46. important source of animal genuine protein ftp://ftp.sp.gov.br/ftppesca/Casali31_1.p for humans. Also, in the major hotels of most df of African countries, H. occipitalis is the best- Channing A. 2001. Amphibian of Central and selling species because it is easy to harvest Southern Africa. Cornell University and has a fairly large thigh with a significant Press, Ithaca, New York, 496pp. economic value. www.cornellpress.cornell.edu/book/?GC OI=80140100275230 COMPETING INTERESTS DDC (Direction du Développement et de la The authors declare that there is no Coopération), 2010. Un seul monde ; competing interests. N°3/ le magazine de la ddc sur le développement et la coopération, 36p. AUTHORS’ CONTRIBUTIONS www.ddc.admin.ch All authors have made adequate effort Dekeyser PL, Villiers A. 1956. Contribution à on all parts of the work necessary for the l'étude du peuplement de la Mauritanie. development of this manuscript according to Notations écologiques et his expertise. All authors read and approved biogéographiques sur la faune de l'Adrar. the final manuscript. Mém. Inst. Franc. Afr. Noire, 44: l- 222. REFERENCES https://www.researchgate.net/.../Catalogu Aisien MSO, Aigbirior PO, Ovwah E, Edo- e-des-Mammiferes- Taiwo O. 2014. Blood parasites of some Dubois A. 1992. Notes sur la classification Anurans from southern Nigeria. Tropical des Ranidae (Amphibiens anoures). Bull. Biomedicine, 32(4): 598–607. Mens. Soc. Linn. Lyon, 61: 305-352. https://www.researchgate.net/.../2906500 https://www.persee.fr/doc/linly_0366- 20_Blood_parasites_of_s... 1326_1992_num_61_10_11011 Akani1 GC, Luiselli L, Amuzie CC, Wokem Ezemonye L, Enuneku A. 2005. Evaluation of GN. 2011. Helminth community acute toxicity of cadmium and lead to structure and diet of three Afrotropical amphibian tadpoles (toad: Bufo anuran species: a test of the interactive- maculatus and frog: Ptychadena versus-isolationist parasite communities bibroni). Journal of Aquatic Sciences, hypothesis. Web Ecol., 11: 11–19. 20(1): 33-38. https://doi.org/10.5194/we-11-11-2011 http://dx.doi.org/10.4314/jas.v20i1.2003 Alfredo S. 1996. Amphibians of Northwest 6 Africa. Smithsonian Herpetological Ezemonye L, Enuneku A. 2011. Biochemical Information. Service. No. 109. 45p. Alterations in Hoplobatrachus citeseerx.ist.psu.edu/viewdoc/download? occipitalis Exposed to Sub Lethal doi=10.1.1.455... Concentrations of Cadmium. Turkish Barbault R. 1984. Stratégie de reproduction et Journal of Fisheries and Aquatic démographie de quelques amphibiens Sciences 11: 485-489. Doi: anoures tropicaux. Oikos, 43: 77-87. 10.4194/1303-2712-v11_3_21 Doi: 10.2307/3544248 FAO. 2016. Situation mondiale des pêches et Burton RV. 1972. Croos-sex Identity in de l’aquaculture. 227p. www.fao.org/3/a- Barbados. Developmental Psycology 6 : i5555f.pdf 365-374. Doi: 10.1037/h0032580 Frost DR. 1985. Amphibians Species of the Casali AP, Moura OM, Lima SL, Silva JHV. World Lawrence, Kansas: allen Press 1490

T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018

and Assoc. Syst. Coll, 1987 (3): 830-833. 64. Doi: 10.2307/1445694 https://amphibiaweb.org/refs/roedel.html Frost DRT, Faivovich J, Bain RH, Haas A, IUCN. 2014. (International Union for Haddad CFB, De Sà RO, Channing A, Conservation of Nature) & Conservation Wilkinson M, Donnellan SC, Raxworthy International. Hoplobatrachus CJ, Campbell JA, Blotto JD, Green occipitalis. The IUCN Red List of Wheeler WC. 2006. The Amphibian tree Threatened Species. Version 2016-2. of life. Bulletin of the American of www.iucnredlist.org/ Natural History, 297: 1–370. James SM, Little EE. 2003. The effects of taxonomicon.taxonomy.nl/Reference.asp cadmium exposure on the American x?id=5337 toad, Bufo americanus tadpoles. Grushwitz MS, Moormann S, Kromer G, Environmental Toxicology and Gietrich H, Boeck G, Gershwin ME, Chemistry, 22: 377-380. Boyd R, Wick G. 1991. Phenotypic https://doi.org/10.1002/etc.5620220219 analysis of skin infiltrates in Kühn ER, Gevaerts H, Jacobs G, Vandorpe G. comparaison with peripheral blood 1987. “Reproductive cycle, thyroxine lymphocytes, spleen cell and thymocytes and corticosterone in females of the giant in early avian scleroderma. J Autoimmun swamp frog Dicroglossus occipitalis at 4: 577-593. the Equator”. General and Comparative https://www.sciencedirect.com/science/a Endocrinology, 66 : 137-144. DOI : rticle/.../0738081X949029... https://doi.org/10.1016/0016- Guerry AD, Hunter JM. 2002. Amphibian 6480(87)90358-3 distributions in a landcape of forest and La Fondation Droit Animal (LFDA), Éthique agriculture: an examination of landcape & Sciences. 2011. Droit animal éthique composition and configuration. & sciences. Revue trimestrielle de la Conservation Biology, 16: 745-754. Fondation LFDA. 32p. www.fondation- https://pdfs.semanticscholar.org/.../c54ae droit-animal.org/documents/revue92.pdf b6553f593c602c6d55630... Lescure J. 1971. L’alimentation du crapaud Heyer WR, Donnelly MA, Mcdiarmid RW, Bufo regularis Reuss et de la grenouille Hayek LAC, Froster MS. 1994. Dicroglossus occipitalis (Günther) au Measuring and Monitoring Biological Sénégal. Bulletin de l’Institut Diversity. Standard Methods for Fondamental d’Afrique Noire, 33: 446– Amphibians. Smithsonian Institution 466. Press: Washington & London; 364p. Loveridge A. 1942. Revision of the Afro- https://pubs.er.usgs.gov/publication/5200 oriental geckos of the genus Phelsuma. 175 Bulletin of the Museum of Comparative Idowu ET, Amaeze NH, Adie PI, Otubanjo Zoology, 89: 439 – 482. OA. 2014. Heavy metal bioaccumulation Loveridge A. 1955. A second collection of and biomarkers of oxidative stress in the reptiles and amphibians taken in wild African tiger frog, Hoplobatrachus Tanganyika territory by C. J. P. Ionides. occipitalis. African Journal of Esq. J. E. Arf. Nat. Hist. Soc., 22: 168- Environmental Science and Technology, 198. 8(1): 6-15. DOI: 10.5897/AJEST2013. www.biodiversitylibrary.org/.../XXII_N 1603 0.5_97__168_1955_Love. Inger RF, Marx H. 1961. The food of Mady-Goma Dirat I, Kimpoudi C, Mikia M, amphibians. Pp. 1–86 in Mission G.F. de Tsoumou A, Vouidibio J, Pandare D. Witte. Exploration du Parc National de 2012. Study of an Edible Frog of l’Upemba, Institut des Parcs Nationaux Brazzaville: Hoplobatrachus occipitalis: du Congo et du Ruanda-Urundi, Fasc. Ranidae (Günther, 1858). I. Res. J. 1491

T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018

Biological Sci. 1(6) : 10-17. value. West African Journal of Applied https://www.yumpu.com/.../hoplobatrach Ecology, 19(1): 67-76. us-occipitalis-ranidae-isca https://www.ajol.info/index.php/wajae/ar Morin R. 2008. Élevage de la grenouille. ticle/view/77567 Document d’information DADD-10. Parker HW. 1936 Amphibians from Liberia Ministère de l’Agriculture, des Pêcheries and the Gold Coast. Zoologische et de l’Alimentation. 9 p. Mededelingen Leiden, 19: 87-102. http://www.mapaq.gouv.qc.ca/Fr/Peche. research.amnh.org/.../amphibia/.../Parker Neveu A. 2004. La raniculture est-elle une -1936-Zool.-Meded.-Leid... alternative à la récolte ? Etat actuel en Perret JL. 1966. Les amphibiens du France. INRA. Prod. Anim. 17 : 167-175. Cameroun. Thèse de doctorat de https://www6.inra.fr/productions- Neuchâtel, 464p. animales/2004...17/...2004/La- Poynton JC, Broadley DG. 1985. Amphibiens raniculture-est-elle-un... Zambesiaca 2. Ranidae. Ann. Natal Noble GK. 1924. A new Spadefoot Toad from Mus., 27: 115–181. 87-102. the Oligocène of Mongolia with a https://amphibiaweb.org/refs/roedel.html summary of the evolution of the Rödel MO, Spieller M. 2000. Trilingual keys Pelobatidae. American Museum to the Savannah-Anurans of the Comoé Novitates, 132: 1-15. National Parc, Ivory Coast. Stuttgarter http://hdl.handle.net/2246/3217 Beitr. Naturk. Ser. A Nr., 620: 1-31. Nzigidahera B. 2006. Note sur Rödel MO. 1995. Phrynobatrachus francisci Hoplobatrachus occipitalis (Günther), im Comoé-Nationalpark, Elfenbeinküste: espèce comestible au Burundi. Institut Lebensräume, Aktivität und Nahrung in National pour l'Environnement et la der ausgehenden Trockenzeit. Conservation de la Nature (INECN), Salamandra 31: 79–92. Burundi. Bull. Sc. lNE. C. N, 1: 1-14. www.salamandra- bi.chm-cbd.net/biodiversity/bulletin...du- journal.com/index.../1995...31/...roedel- bulletin- m-o-1/fi... deja.../bulletin_1.../1/bulletin_1.pdf Schiøtz A. 1999. The Treefrogs of Africa. Olvera-Novoa MA, Ontiveros-Escutia VM, Series: Edition Chimaira: Chimaira, Flores-Nava A. 2007. Optimum protein Frankfurt am Main, Germany; 350 p. level for growth in juvenile bullfrog research.amnh.org/vz/herpetology/5_6a (Rana catesbeiana, Shaw, 1802). mphibia/?action=bib... Aquaculture, 266(10): 191-199. Scortecci G. 1936. Gli anfibi délia www.academia.edu/.../Optimum_protein Tripolitania. Atti Soc. Ital. Sci. Nat., _level_for_growth_in_juv... 75: 129-226. Omonona AO, Jubril AJ, Akinnibi OF, https://www.researchgate.net/.../Bibliogr Adekola AA. 2016. Cadmium Bio- aphy-of-North-African-Herpetology- Accumulation and the Associated Smithso... Biomarkers in Edible Frog Species Sobha K, Poornima A, Harini P, Veeraiah K. (Hoplobatrachus occipitalis) in Ibadan, 2007. A study on the biochemical Oyo State, Nigeria. World Vet J, 6(2): changes in freshwater fish Catla catla 70-79. wvj.science- exposed to the heavy metal toxicant, line.com/.../World%20Vet.%20J.%206(2 cadmium chloride. Kathmandu )%2070-79,... University Journal of Science, Onadeko AB, Egonmwan RI, Saliu JK. 2011. Engineering and Technology, 1: 4-11. Edible amphibian species: local Spieler M, Linsenmair KE. 1998. Migration knowledge of their consumption in patterns and diurnal use of shelter in a southwest Nigeria and their nutritional ranid frog of a West African savannah: a 1492

T. GODOME et al. / Int. J. Biol. Chem. Sci. 12(3): 1484-1493, 2018

telemetric study. Amphibia-Reptili, 19: www.zobodat.at/.../Bonner-Zoologische- 43-64. Doi: 10.1163/156853898X00322 Beitraege_30_0385-0403.... Tohé B, N’Guessan EA, N’Goran GK. 2016. Volgiatzis AK, Loumbourdis N. 1997. Reproduction of African Tigrine Frog Uptake, tissue distribution and Hoplobatrachus occipitalis in Banco depuration of cadmium (Cd) in the frog National Park (Ivory Coast). Rana ridibunda. Bulletin of International Journal of Science and Environmental Contamination and Research (IJSR). 5(1): 2319-7064. Toxicology, 59: 770-776. https://www.ijsr.net/archive/v5i1/NOV1 Wells KD. 1977. The social behaviour of 52680.pdf anuran amphibians. Animal Behaviour, Tohé B. 2009. Reproduction et régime 25: 666-693. alimentaire de trois espèces d’anoures http://dx.doi.org/10.1016/0003-3472 des habitats dégrades du Parc National (77)90118-X du Banco (Côte d’Ivoire): Ptychadena Whitfield SM, Bell KE, Philippi T, Sasa M, mascareniensis, P. pumilio et Bolaños F, Chaves G, Savage JM, Hoplobatrachus occipitalis. – PhD thesis, Donnelly MA. 2007. Amphibian and Université d’Abobo-Adjamé, Abidjan, reptiles declines over 35 years at La Côte d’Ivoire, 132 p. Selva, Costa Rica. PNAS, 104(20): 8352- van den Elzen P, Kreulen DA. 1979. Notes on 8356. DOI: 10.1073 / pnas.0611256104 the vocalisations of some amphibians Zug GR. 1987. Amphibians and reptiles of the from the Serengeti National Park, Outamba-Kilimi region, Sierra-Leone. J. Tanzania. Bonner zoologische Beiträge, Herpetol. Ass. Afr., 33 : 1-4. DOI: 30: 385–403. 10.1080/04416651.1987.9650167

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