This study reviewed the survey of malformed frogs and the probable causes of their deformities. It analysed the checklist and pattern of malformations in frogs and examined different malformations in frogs of selected articles. It also reviewed the causes of malformation in frogs of different articles. The reviewed showed that limb malformations with 22.41% was the most recorded malformations in frogs with pattern of publications revealed that there was varying trend in article publication which peaked in 2000 and 2023. Different malformations in frogs are abnormal skin, albinism, extra hindlimb, eye malformation. Others are lack of palms, appendages and appendicular, limb malformation, ectrodactyly, brachydactyly and ectrodactyly. The causes of malformations in frogs reviewed includes mutation, parasites, heavy metals, environmental stressors and ultraviolet light. The study concluded that human factors or anthropogenic activities played an important role in malformations in frogs reviewed.

Keywords: frogs, deformities, ectrodactyly, brachydactyly, ectrodactyly

A frog is any member of a diverse and largely carnivorous group of short-bodied, tailless amphibians composing the Order Anura.¹ Warty frog species tend to be called toads, but the distinction between frogs and toads is informal, not from taxonomy or evolutionary history.² Anurans mostly lay their eggs in water, breed by producing tadpoles that develop there, and eventually become amphibious adults.³ They constitute an excellent indicator for monitoring the environment due to their complex life cycles and high sensitivity to environmental changes.⁴ Frog populations have declined over the past 20 years due to habitat loss and degradation, increased pollution, and changes in the global climate (Rodriguez and Fernandez, 2005). Malformed frogs are a significant problem in addition to the quick decreases in frog populations.⁵ Mass population depletion and odd occurrences like deformities are signs that our environment may be facing crises.⁶

The presence of other toxins in the water, such as heavy metals like copper, xenoestrogens like diethylene glycol, and pesticides like methoxychlor, may result in the development of deformed frogs.⁷ Frog deformity can be caused by parasite Ribeiroia ondatrae infection in addition to increasing UV radiation and water pollution.⁸ Numerous deformed frogs have been reported in the US and Europe.^9–11 Wildlife has an intrinsic strategy to live in the most unlikely situations when faced with xenobiotic pollutants that impact them, such as changes in enzyme activity or protein expression.¹² The aim of this study is to review the survey of malformed frogs and the probable causes of their deformities.

Studies on amphibian limb abnormalities have recently become common in the field of amphibian conservation. These abnormalities can vary from limb malformations to complete limb absence. Many stressors can cause similar responses and a singular cause that links the array of abnormalities is not known. Instead, the several known causes of these abnormalities appear to have variable effects. Malformations are deformities that are caused by environmental factors which prevent normal anatomical development, especially during the larval life-stage. As a result, affected animals can develop too many, or not enough, of certain body parts.¹³

Different authors have reported malformations in frogs and toads. Meteyer et al.¹⁴ recorded abnormalities in northern leopard frogs Rana pipiens and it is most commonly found in Minnesota. Their investigation showed that 6.5 % of 13,763 frogs collected were malformed. The malformations observed included missing limbs, missing digits, extra limbs, partial limbs, skin webbing, malformed jaws, and missing or extra eyes. Schoff et al.¹⁵ also recorded the prevalence of skeletal and eye malformations in frogs from North-Central, United States. The results revealed that 2.3% of the total population had eye malformations while 1.6% recorded skeletal malformations. It has also been reported that internal organs can be affected but amphibian malformations noticed by the public are usually those affecting external body parts, such as digits, limbs or the tail in newts and salamanders.¹⁶ A variety of agents are known to cause malformations in amphibians, these include pollutants, parasites, nutritional deficiencies and injury during development. Other possible causes of amphibian deformations are genetic and environmental factors, such as microbial diseases and other disorders, elevation of UV-B radiation and the major chemical agents, most of them found in agribusiness pollution.¹⁷ These may cause homeostatic imbalances that can result in incorrect developments of anurans.¹⁸ Lannoo¹⁹ argued that many sources, both natural and artificial, ranging from fish excrement to overcrowding, are significant when pinpointing causes of the abnormalities. Malformations detected in different anurans inhabiting different microhabitats may denote environmental complications, which also may impact on other organisms and are important to help understanding malformation dynamics.²⁰

Studies on Frog Malfunction

Amphibians’ population have been recorded to be on the decline since the 1980s. According to Whitfield et al.,²¹ this development has led to the current biodiversity crisis. It has also been documented that decrease in the population could be as a result of developmental malformations, especially limb deformities, occurring in amphibians.²² The authors are of the view that normal rate of abnormalities which was 5% and occur naturally had increased to 15%. Amphibians have moist, permeable skins and shell-less eggs which are directly exposed to the soil, water and sunlight, and can absorb toxic substances present in their surrounding environment.²³ These toxic substances have been known to cause different types of abnormalities in amphibians.²⁴

Amphibians are especially sensitive to changes in precipitation, temperature and ultraviolet radiation and their habitats may be influenced strongly by acid precipitation.²⁵ Thus, amphibians are considered to be excellent biological indicators of general environmental health and early warning systems to environmental degradation.²³ Abnormalities in frogs have been conducted through surveys and experimental studies. In a study conducted by Farquharson et al.²⁴ on the impacts of toxin on the four frog species of found in protected areas of Kruger National Park. The results showed that frogs exhibited deformities in different parts of their body. In a field survey conducted by Thigpen et al.,²⁶ sixteen Fowler’s toads, Anaxyrus fowleri, and one dwarf American toad, Anaxyrus americanus charlesmithi were collected in central Arkansas through direct observation of abnormal toads. Their findings revealed varying degree of abnormalities in both forelimbs and hindlimbs and on both sides of the body. The study concluded that the environment might have caused the abnormalities recorded in the frogs.

Similarly, Mônico et al.²⁷ reported malformation in three anuran species from a preserved remnant of Atlantic Forest in southeastern Brazil. The frog species investigated are Crossodactylus timbuhy, Proceratophrys schirchi and Thoropa miliaris. The study showed that malformations detected in frogs were hemimelia (long bone shortened with ectrodactyly digit absent) and brachydactyly (digit shortened) in C. timbuhy while microphtalmia (small eye) was reported in P. schirchi and ectrodactyly in T. miliaris. A report on morphological malformation of adult Itapothyla langsdorffii in Rebio reserved area, south eastern Brazil, was carried out by Mônico et al.²⁷ The study reported an individual with a malformed head during the survey period. Lunde and Johnson¹³ was of the view that amphibians in well-preserved areas can have natural osteological deformities as a consequence of intrinsic genetic and developmental imperfections. Two hundred and ninety-three Lithobates spp. of frogs collected from wetlands in an agricultural region of Nebraska, USA were examined for abnormalities. The frogs showed gonadal anomalies and results revealed that the froglets had ovarian dysgenesis and high rates of testicular oocytes. Ballengee and Sessions¹⁸ provided evidence experimentally supporting the idea that missing limbs in deformed amphibians can be caused by a specific predator. It was reported that dragonfly nymphs use sublethal ‘‘selective predation,’’ attacking or capturing tadpoles and gnawing off their protruding hind limbs, often causing permanent limb deformities in frogs that survive to metamorphosis.

Studies have also shown that deformed frogs featuring extra limbs are caused by a parasite, specifically the trematode Ribeiroia ondatrae.²⁸ Ballengee and Session¹⁸ observed that tadpoles with deformities caused by parasites such as extra limbs are largely immobile and do not survive long once they metamorphose. Pollutants such as chemical pollutants have been shown to cause limb deformities in natural populations of amphibians.²⁹

Survey of malformation in African frogs

The current widespread deformities among frogs seem to have been linked to recent environmental changes. Numerous amphibian population declines have been attributed to increased mortality rates following infection with the pathogenic chytrid fungus Batrachochytrium dendrobatidis.³⁰ Other factors associated with the amphibian decline phenomenon include habitat loss, climate change, infectious disease, overexploitation, pollution and introduced species.³¹ A study to determine the effect of atrazine application on the African clawed frog (Xenopus laevis) inhabiting ponds in a maize-growing area MGA and non-maize-growing area NMGA in the Viljoenskroon and Potchefstroom regions of South Africa was investigated by Du Preez et al.³² The results showed that the herbicide atrazine caused gonadal deformities in frogs.

Amphibians play diverse roles in natural ecosystems and their decline may cause other species to become threatened or may undermine aspects of ecosystem function.³³ Frogs are an important prey source for diverse predators and their tadpoles, which are usually filter feeders, contribute to the stability of water quality in ponds and streams Mohneke et al.,³⁴ In a study conducted by Ezemonye and Tongo,³⁵ Bufo regularis was evaluated to determine the uptake and effect of environmentally toxicity of Endosulfan and Diazinon pesticides. The results of the authors showed that the pesticides caused dose-dependent deformities and behavioural abnormalities in Bufo regularis.

Malformation in Nigerian frogs

Nigeria is located within the Guinean rain forest GrF biodiversity hotspot of West Africa. It is located between West and Central Africa.³⁶ Thus, the country is situated between the biodiversity hotspot of the upper and lower Guinea forest regions.³⁶ Nigeria boasts of a wide variety of ecosystems ranging from mangroves and rainforests in the south, different savannahs up north, to the Jos plateau in central Nigeria and mountainous habitats in Eastern Nigeria towards the Cameroon border.³⁷ About 115 species of amphibians have been recorded within the country, two of which are caecilians and one endemic species Amietophrynus perreti has been described in the country.³⁸

A high biodiversity loss including steep decline in amphibian populations has necessitated assessment of the conservation status of amphibians in Nigeria. The causes of amphibian population declines are diverse and there appears to be no single cause for their decline.³⁹ Nigeria harbours high biodiversity and endemism consisting of both West and Central African Anuran species.³⁷ Nigeria is also blessed with amphibian biodiversity which are observed in areas around waterbodies.⁴⁰ Though, some regions have been documented to be seriously affected by pollution especially in the Niger Delta region. There is high tendency that anurans especially in that region of Nigeria would have undergo some abnormalities.

Abnormalities in amphibians have been reported around the world in a broad number of taxa,⁴¹ but there is little or no literature on malformation or abnormalities in Nigeria frogs. However, toad abnormalities have been documented to some extent in Nigeria. Akinsanya et al.⁴² examined the impacts of trace metals on the African common toad, Amietophrynus regularis in Lagos Lagoon. A total of 120 toads of both sexes, alongside 45 soil samples were collected from each of three 3 stations labeled Dumpsite, Lagoon front and Highrise, using hand nets and by hand-picking. The results showed that there were mild tissue alterations in the toads analysed.

Many factors influence the development of morphological abnormalities in amphibians, such as genetic predisposition, heavy metal concentrations, radiation exposure.⁴³ Synergistic interactions of these factors have also been documented to influence malformations.⁴⁴ Rates of abnormalities are considered natural when present in less than 5% of the population (Stocum, 2000). Amphibians play important roles in ecosystem services, medical research and as bio-indicators. Yet, nearly 41% of all existing amphibians are threatened with extinction due to factors such as abnormalities, diseases, human activities.

Methodology

This involved finding citations made on malformations in natural populations of frogs. The literature on malformation of frogs were compiled through various sources of citation. This study also involved extensive collection of literatures related to frog malformations from different sources such as research gate, academia, Z-library, google scholar etc. Keywords such as frog deformity, malformation, anuran abnormality and frog defects were used to obtain researches published between 1990 and 2023. Examining the occurrence of malformations presents significant difficulties because obvious physical malformations in one species may be the norm in another. Injuries in our counts of malformations were included because they can result in malformed structures and can be challenging to distinguish from other developmental malformations. Only journals that are related to abnormalities were included. Different varying degrees of abnormalities were recorded based on their years of reportage. The frequency of malformations was also analysed with respect to the different frog species and their corresponding references. Causes of the abnormalities and their corresponding abnormalities were also reviewed in order to understand the different causes of anomalies.

Checklist of Malformations in frogs

The checklist of malformation showed that limb malformation was the most recorded malformations. Other malformations that recorded numerical reportage by authors are eye malformation, abnormal skin, hindlimb malformation and ectrodactyly as presented in Table 1. The pattern of publications of different malformations showed that it ranged from 1993 with a peak period in 2000. However, there was a little downward trend in 2003 and 2010. Also, increase in reportage was also observed in 2017 with highest level recorded in 2022 as shown in Figure 1,2. The percentage of malformations in frog revealed that limb malformation had the highest reported malformation while malformations such as brachydactyly, skin and limb rotation and mouth malformation were among the least reported malformations as presented in Table 2.

Figure 1 Pattern of Publications Reportage of Malformations in Frogs.

Figure 2 Some common malformations observed in frogs; A: Missing limb. B: Incompletely formed hindlimbs. D: malformed hindlimb. C, E and F: Extra limb.

Malformations in different frogs

Different malformations were recorded in different frogs by different authors as shown in Table 3. Frog species such as Amolops chunganensis, Rana clamitons, Scinux squalirostris, Rana marina were reported with different malformations. The malformations included abnormal skin, albinism, hindlimb malformation, limb abnormalities etc. others are absence of eyes or eye malformation, split-leg malformation, polydactyly, missing digits of varying severity. These digits severity recorded are oligodactyly, ectrodactyly and brachydactyly. The frequency of malformations showed that different authors recorded frequency of occurrence that varied from 0.01% in Rana temporaria to 100% in Rana hanluica.

Rana pipiens recorded 86% hindlimb malformation while 81% malformation of the limb was reported in Rana catesbeina. The tree summary of different abnormalities in frogs showed that limbs malformation and its associated severity were the most reported malformations while eye malformation was the least recorded abnormalities as shown in Figure 3&4.

Figure 3 Tree Summary of Malformations in Reported Frogs.

Figure 4 Causes of frog abnormalities.

Causes of Abnormalities

The parasite Ribeiroia ondatrae has been observed to cause limb malformation in frogs. Heavy metals also cause eye malformation while polymely is caused by chemicals or mutagenic factors. Limbs and ocular malformation, lack of palms, appendages exostosis to appendicular and skin abnormalities are caused by environmental stressors, organic pollutants and agricultural chemicals and mechanical perturbation respectively as shown in Table 4.

Malformation of frogs have been a major interest since the 1990s when some students observed some malformed frogs when on tour.¹⁰³ This gave rise to more focus and prompted researchers to examine malformations in frogs and its causes since the 1990s. The reviewed malformations of frogs of this current study showed that 1990s was the period of most documented reports on malformed frogs which peak in 2000. According to Loeffler et al.,¹⁰⁴ the investigation of malformations in frogs has underscore the wide range in the different malformations in frogs. Most of the observed malformations reviewed in this study were limb, eye, and skin malformations. Also, varying degree in severity of limb malformations was also recorded such as ectrodactyly, polymelia, brachydactyly etc. Polymelia and ectrodactyly in different frog species have been documented to be caused by parasite trematode worm from genus Ribeiroia.^97,105 This parasite physically or chemically disrupts the developing limb, jaw or eye fields.¹⁰⁶ Albinism which was documented in frogs is caused by several different genes.¹⁰⁷

Also, limb malformations were the most documented frog malformations by different authors. Thus, available data suggests that limb malformations could be used as a baseline malformation for frogs of different species. Evidence has shown that water contamination, pesticides, herbicides, petrochemicals and UV radiation could results to abnormities in frogs (Johnson et al., 2000).¹⁰⁸ This reviewed also showed that malformations in frogs were documented among different species of frogs and evidence showed that malformation in different frogs are not species specific. Different causes of malformations have been documented for different frog species. Although no single cause has been found to explain all frog malformations. However, mutation, parasite, environmental stressors, organic pollutants have been recorded as causes of malformation in frogs.^75,102 These chemicals are known to act as retinoids which are potent regulators of development in the vertebrate brain, eye, mandible and limbs.¹⁵ In conclusion, this study gave an insight into the malformation of frogs from 1990 to 2023. The study reviewed that limb malformation was the most occurred abnormalities among the different frogs. The study concluded that human factors or activities played an important role in frog malformations. Although malformations in frogs cannot be completely stopped, there is need to completely reduce anthropogenic activities which may mitigate the problem. Further researches need to be carried out to determine the exact cause of each deformity that has been observed in frogs and it is recommended that the indiscriminate dumping of toxic waste, use agrochemicals such as pesticides, and harmful chemicals should be discouraged and made illegal.^109–116

None.

The author declares there is no conflict of interest.

1. Frost DR. Amphibian Species of the World: Version 6.1. American Museum of Natural History, New York. 2021.
2. Laurie JV, Janalee PC. Chapter 17 – Frogs. 2014. p. 471–522.
3. McDiarmid R, Altig RW. Diversity: In McDiarmid. et al., editors. Tadpoles: The Biology of Anuran Larvae. University of Chicago Press, Chicago, Illinois, U.S.A familiar and generic characterizations. 1999;295–337.
4. Venturino A, Rosenbaum E, Caballero de Castro A. et al. Biomarkers of effect in toads and frogs. Biomarkers. 2003;8(3–4):167–186.
5. Loman J, Andersson G. Monitoring brown frogs Rana arvalis and Rana temporaria in 120 south Swedish ponds 1989-2005. Mixed trends in different habitats. Biological Conservation. 2007;135:46–56.
6. Kiesecker JM. Global stressors and the global decline of amphibians: tipping the stress immunocompetency. Axis of Ecological Research. 2011;26(5):897–908.
7. Fort DJ, Thomas JH, Rogers RL, et al. Evaluation of the developmental and reproductive toxicity of methoxychlor using an anuran (Xenopus tropicalis) chronic exposure model. Toxicological Sciences. 2004;81(2):443–453.
8. Johnson PTJ, Lunde KB, Haight RW, et al. Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology. 2001;79(3):370–379.
9. Geer K, Krest S. A new threat to frogs. Endangered Species Bulletin. 2000;25:12–13.
10. Meteyer CU. Field guide to malformations of frogs and toads with radiographic interpretations. In: Biological Science Report USGS/BRD/BSR–2000–0005. 2000.
11. Vandenlangenberg SM, Canfield JT, Magner JA. A regional survey of malformed frogs in Minnesota (USA)(Minnesota malformed frogs). Environmental Monitoring and Assessment. 2003;82:45–61.
12. Bhattacharya S. Stress response to pesticides and heavy metals in fish and other vertebrates. Proc. Indian Natn. Sci. Acad. (PINSA) B67, 215e246. 2001.
13. Lunde KB, Johnson PT. A practical guide for the study of malformed amphibians and their causes. Journal of Herpetology. 2012;46:429–442.
14. Meteyer CU, Loeffler IK, Fallon JF, et al. Hind limb malformations in free-living northern leopard frogs (Rana pipiens) from Maine, Minnesota, and Vermont suggest multiple etiologies. Teratology. 2000;62(3):151–71.
15. Schoff PK, Johnson CM, Schotthoefer AM, et al. Prevalence of skeletal and eye malformations in frogs from north-central United States: estimations based on collections from randomly selected sites. Journal of Wildlife Diseases. 2023;39(3):510–521.
16. McCallum ML, Trauth SE. A forty-three-year museum study of northern cricket frog (Acris crepitans) abnormalities in Arkansas: upward trends and distributions. Journal of Wildlife Diseases. 2003;39(3):522–528.
17. Koleska D, jablonski D. Two cases of unclear hindlimbs in malformation in Bombina Variegata. Ecologica Montenegrina. 2016;9:56–58.
18. Ballengee B, Sessions SK. Explanation for missing limbs in deformed amphibians. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2009;312(7):770–779.
19. Lannoo M. Malformed Frogs. The Collapse of Aquatic Ecosystems. University of California Press, Berkeley – Los Angeles – London. 2008.
20. Johnson ML, Berger L, Philips L. Fungicidal effects of chemical disinfectants, UV light, dessication and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organism. 2003;57:255–260.
21. Whitfield SM, Bell KE, Phillipi T, et al. Amphibian and Reptile declines over 35years at la Selva, Costa Rica. Proc Natl Head sci. 2007;104(20):8352–8656.
22. Johnson PTJ, Lunde KB. Parasite infection and limb malformations: a growing problem in amphibian conservation. In: Amphibian Declines: the Conservation Status of United States Species. In: Lannoo MJ, et al., editors. California, USA, University of California Press. 2005. p. 124–138.
23. Huang H, Wang X, OU W, et al. Acute toxicity of benzene derivatives to the tadpoles (Rana japonica) and QSAR analyses. Chemosphere. 2003;53(8):963–970.
24. Farquharson C, Wepener V, Smit NJ. Acute and chronic effects of acidic pH on four subtropical frog species. Water SA. 2016;42(1):52–62.
25. Horne MT, Dunson WA. Effects of low pH, metals, and water hardness on larval amphibians. Archives of Environmental Contamination Toxicology. 1995;29:500–505.
26. Thigpen CS, Beard D, Trauth SE. Toad (Anura: Bufonidae) limb abnormalities from an aquatic site in Scott, Pulaski County, Arkansas. Journal of the Arkansas Academy of Science. 2014;68(1):106–109.
27. Mônico AT, Silva-Soares T, Koch ED. Malformation in three anuran species from a preserved remnant of Atlantic Forest in southeastern Brazil. Neotropical Biology and Conservation. 2019;14(2):213–220.
28. Stopper GF, Hecker L, Franssen RA, et al. How trematodes cause limb deformities in amphibians. Journal of Experimental Zoology. 2002;294:252–63.
29. Ankley GT, Degitz SJ, Diamond SA, et al. Assessment of environmental stressors potentially responsible for malformations in North American anuran amphibians. Ecotoxicology and Environmental Safety. 2004;58(1):7–16.
30. Lips KR, Brem F, Brenes R, et al. Emerging infectious disease and the loss of biodiversity in a Neotropical Amphibians community. PNAs. 2006;103:3165–3170.
31. Beebee TJ, Griffiths RA. The Amphibian Decline Crisis: A Watershed for Conservation Biology? Biological Conservation. 2005;125(3):271–285.
32. Du Preez LH, Solomon KR, Carr JA, et al. Population structure of the African clawed frog (Xenopus laevis) in maize-growing areas with atrazine application versus non-maize-growing areas in South Africa. African Journal of Herpetology. 2005;54(1):61–68.
33. Whiles MR, Lips KR. The effects of amphibian population declines on the structural and function of Neotropical stream ecosystems. Front Ecological Environment. 2006;4:27–34.
34. Mohneke M, Onadeko AB, Hirschfeld M. Dried or fried: amphibians in local and regional food markets in West Africa. Traffic Bulletin. 2010;22(3):117–128.
35. Ezemonye L, Tongo I. Acute toxic effects of endosulfan and diazinon pesticides on adult amphibians (Bufo regularis) Journal of Environmental Chemistry and Ecotoxicology. 2010;2(5):73–78.
36. Bakarr M, Oates JF, Fahr J, et al. Guinean forests of West Africa. – pp. 123-130 in: Herpetofauna of Gashaka Gumti National Park, Nigeria. 2004. p. 553.
37. Onadeko AB, Rodel MO. Anuran surveys in Southwestern Nigeria, West Africa. Salamandra. 2009;45:1–14.
38. Nneji LM, Adeniyi AC, Fang Y. Cryptic diversity of Nigerian Agama within West African radiation. Russian Journal of Herpetology. 2018;25(2):97–112.
39. Blaustein AR, Walls SC, Bancroft BA, et al. Direct and indirect effects of climate change on amphibian populations. Diversity. 2010;2(2):281–313.
40. Nneji LM, Adeola AC, Okeyoyin AO, et al. Diversity and distribution of amphibians and reptiles in Gashaka Gumti National Park, Nigeria. Herpetology Notes. 2019;12:543–599.
41. Wagner N, Lötters S, Veith M, et al. Acute toxic effects of the herbicide formulation Focus Ultra on embryos and larvae of the Moroccan painted frog, Discoglossus scovazzi. Archives of environment contamination and toxicology. 2000;69:535–544.
42. Akinsanya B, Isibor PO, Onadeko B, et al. Impacts of trace metals on African common toad, Amietophrynus regularis (Reuss, 1833) and depuration effects of the Amietophrynus regularis enteric parasite, Amplicaecum africanum (Taylor, 1924) sampled within Lagos metropolis, Nigeria. Heliyon. 2020;6(3):e03570.
43. Correia LL, de Almeida JP, Lisboa BS, et al. Brachydactyly in the toad Rhinella granulosa (Bufonidae) from the Caatinga of Brazil: a rare case with all limbs affected. Herpetology Notes. 2018;11:445–448.
44. Johnson PT, Preu ER, Sutherland DR, et al. Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations. Ecology. 2006;87:2227–2235.
45. Sun D, Ellepola G, Herath J, et al. New climatically specialized lineages of Batrachochytrium dendrobatidis and their sub-lethal effects on amphibians establish the Asiatic origins of the pathogen. BioRxiv. 2023;202–2-01.
46. Roberts CD, Dickinson TE. Ribeiroia ondatrae causes limb abnormalities in a Canadian amphibian community. Canadian Journal of Zoology. 2012;90(7):808–814.
47. Hoppe DM. Malformed frogs in Minnesota: history and interspecific differences. Amphibian declines: The conservation status of United States species. 2005;103–108.
48. Miura I, Tagami M, Fujitani T, et al. Spontaneous tyrosinase mutations identified in albinos of three wild frog species. Genes and Genetic Systems. 2017;92(4):189–196.
49. Johnson PT, Sutherland DR. Amphibian deformities and Rebeiroia infection: an emergency helminthiasis. Trends in parasitology. 2003;19(8):332–335.
50. Rivera X, Arribas O, Martí F. Review of pigment anomalies in amphibians of the Iberian Peninsula and Europe. Bulletin Soc Cat development Herpetology. 2001;15:59–75.
51. Katz AV. On findings of colour anomalies in the moor frog Rana arvalis :Nilsson, 1842. (Ranidae, Amphibia) in the Moscow region. Current Studies in Herpetology. 2022;22(1–2):65–69.
52. Seabrook-Davison MN, Seabrook-Davison J, Brunton DH. Discovery of a green frog Litoria aurea with five webbed feet-amphibian deformities and consequences for the conservation of native and introduced frogs. Pacific Conservation Biology. 2010;16(4):270.
53. Helgen JC, Gernes MC, Kerten SM, et al. Field investigations of malformed frogs in Minnesota 1993–97. Journal of the Iowa Academy of Science. 2009;107(3–4):96–112.
54. Eaton BR, Eaves S, Stevens C, et al. Deformity levels in wild populations of the Wood Frog (Rana sylvatica) in three ecoregions of western Canada. Journal of Herpetology. 2004;38(2):283–287.
55. Lalremsanga HT. Anopthalmia in a Greater Stream Horned Frog, Xenophrys major (Boulenger, 1908), from Tamdil National Wetland, Mizoram, India: Pollution-induced or predator-mediated?. Reptiles and Amphibians. 2022;29(1):201–203.
56. Heinicke MP, Duellman WE, Hedges SB. Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(24):10092–10097.
57. Silva-Soares T, Mônico AT. Hind limb malformation in the tree frog Corythomantis greeningi (Anura: Hylidae). Phyllomedusa. 2017;16(1):117–120.
58. Quellet M, Bonin J, Rodrigue J, et al. Hindlimb wildlife diseases, (ectromelia, ectrodactyly) in free-living anurans from agricultural habitats. Journal of Herpetology. 1997;33(1):95–104.
59. Siammawii V, Malsawmdawngliana F, Muansanga L, et al. Hindlimb malformation in a Bangladesh Skittering Frog, Euphlyctis kalasgramensis Howlader, Nair, Gopalan, and Merila 2015 (Anura: Dicroglossidae). Reptiles and Amphibians. 2022;29(1):195–196.
60. Huang DJ, Chiu YW, Chen CM, et al. Prevalence of malformed frogs in Kaoping and Tungkang river basins of southern Taiwan. Journal of Environmental Biology. 2010;31(3).
61. Volpe EP, Rosenbaum PA. Understanding evolution. Publisher. McGraw-Hill. Language. English. 2000. p. 258.
62. Yeung HY, Yang, JH. Limb malformation and ocular abnormalities in a Large Odorous Frog, Odorrana graminea (Boulenger, 1899) (Anura: Ranidae). Reptiles and Amphibians. 2022;29:101–108.
63. Sower SA, Reed KL, Babbitt KJ. Limb malformations and abnormal sex hormone concentrations in frogs. Environmental Health Perspectives. 2000;108(11):1085–1090.
64. Piha H, Pekkonen M, Merilä J. Morphological abnormalities in amphibians in agricultural habitats: a case study of the common frog Rana temporaria. Copeia. 2006;(4):810–817.
65. Gardiner DM, Hoppe DM. Environmentally induced limb malformations in mink frogs (Rana septentrionalis). Journal of Experimental Zoology A 1999;284(2):207−216.
66. Jorgewich-Cohen Gabriel, Cavalcanti Isabela RS, Kanasiro André. Abnormalities in hylid frogs: a case study of schizodactyly in the striped snouted treefrog, Scinax squalirostris (Lutz, 1925) (Amphibia: Anura: Hylidae). Herpetology Notes. 2019;20–23.
67. Pommer-Barbosa RA, da Cruz EN, Reis JF, et al. Report on a morphological malformation in Boana cinerascens (Spix, 1824) from the southwestern Brazilian Amazon (Anura, Hylidae). Herpetology Notes. 2022;15:237–238.
68. Jaman MF, Sarker MAR, Rana SA. Limb malformation in the skipper frog (Euphlyctis cyanophlyctis) (Amphibia: Dicroglossidae), first evidence in Bangladesh. Herpetological Bulletin. 2017;141:41.
69. Alvarez JA, Garten KM, Cook DG. Limb malformation in a foothill yellow-legged frog (Rana boylii) from sonoma county, California. Northwestern Naturalist. 2021;102(3):258–260.
70. Nekrasova OD, Kuibida VV. Researching malformations in frogs of the Pelophylax esculentus Complex (Amphibia: Anura) in the natural popula-tions of the Trakhtemyriv Peninsula (Ukraine). 2018.
71. Hedrick AR, Cossel JR. Limb malformations of the critically endangered stream-breeding frog Isthmohyla Rivularis in the Monteverde Cloud Forest Preserve, Costa Rica. Herpetological Review. 2014;45(1):5–8.
72. Zuluaga-Isaza JC, Marín-Martínez M, Díaz-Ayala RF, et al. First records of limb malformations in a cane toad, Rhinella marina (Anura: Bufonidae), and a Palm Rocket Frog, Rheobates palmatus (Anura: Aromobatidae), from Colombia. Reptiles and Amphibians. 2017;24(2):132–134.
73. Jilani MJ, Rais M, Asadi MA, et al. Comparison of morphometric and gravimetric measurements of Common Skittering Frog (Euphlyctis cyanophlyctis) from paddy fields and urban wetlands. Journal of King Saud University-Science. 2018;30(3):404–411.
74. Garber EA, Erb L, Magner J, et al. Low levels of sodium and potassium in the water from wetlands in Minnesota that contained malformed frogsaffect the rate of Xenopus development. EnvironmentalMonitoring and Assessment. 2004;90(1–3):45–64.
75. Bowerman J, Johnson PT, Bowerman T. Sublethal predators and their injured prey: linking aquatic predators and severe limb abnormalities in amphibians. Ecology. 2010;91(1):242–251.
76. Kryvoltsevych A, Fedorova A, Shabanov D. Anomalies in marsh frogs (Pelophylax ridibundus) and hybrid waterfrogs (P. esculentus) (Anura: Ranidae). from two ponds in the Kharkiv Region of Ukraine. Repiles and Amphibians. 2022;29(1): 204–209.
77. Molina-Betancourt R, Bacheley L, Karapetyan A, et al. An Environmentally Sustainable Synthesis of Enantioenriched CF3-Chromanol, Indanol and Tetralol Derivatives by Rh-Catalyzed Asymmetric Transfer Hydrogenation. Chem Cat Chem. 2022;14:e202200595.
78. Dos Santos S, Adams EA, Neville G, et al. Urban growth and water access in sub-Saharan Africa: Progress, challenges, and emerging research directions. Science of Total Environmental journals. 2017;607–608:497–508.
79. Gray RH. Morphological abnormalities in Illinois Cricket Frogs, Acris crepitans, 1968-71. Journal of the Iowa Academy of Science: JIAS. 2000;107(3–4):92–95.
80. Ibragimova DV, Nakonechnyi NV. Comparative Analysis of Moor Frog Anomalies (Rana arvalis Nils., 1842) in Different Areas of Surgut City. KnE Life Sciences. 2018;65–69.
81. Hassine JB, De Buffrénil V, Nouira S. First record of morphological abnormalities in natural populations of two amphibian species in Tunisia. Journal of Herpetology. 2011;45(4):465–471.
82. Bettaso J. Humboldt bay national wildlife refuge 2004 Northern red-legged frog malformation report. Arcata Fisheries Technical Report AFWO-TR :08-04. 2004.
83. Converse KA, Mattsson J, Eaton Poole L. Field surveys of midwestern and northeastern Fish and Wildlife Service lands for the presence of abnormal frogs and toads. Journal of the Iowa Academy of Science. 2000;107(3–4):160–167.
84. Burger J, Snodgrass JW. Oral deformities in several species of frogs from the Savannah River Site, USA. Environmental Toxicology and Chemistry: An International Journal. 2000;19(10):2519–2524.
85. Rowe CL, Kinney OM, Congdon JD. Oral deformities in tadpoles of the bullfrog (Rana catesbeiana) caused by conditions in a polluted habitat. Copeia. 1998;(1):244–246.
86. Svinin AO, Bashinskiy IV, Osipov VV, et al. New records of the anomaly P syndrome in two water frog species (Pelophylax ridibundus and P. lessonae) in Russia. Herpetozoa. 2019;32:277–281.
87. Read JL, Tyler MJ, Robinson M. Recruitment and abnormality incidence of a desert frog assemblage at an Australian copper mine. Ecological Management and Restoration. 2015;16(3):224–228.
88. Hegde G, Krishnamurthy SV. Analysis of health status of the frog Fejervarya limnocharis (Anura: Ranidae) living in rice paddy fields of Western Ghats, using body condition factor and AChE content. Ecotoxicology and Environmental Contamination. 2014;9(1):69–76.
89. McCallum ML. Rana sphenocephala (Southern leopard frog) malformities found in Illinois with behavioral notes. Transactions of the Illinois State Academy of Science. 1999;92:257–264.
90. Litvinchuk SN. “Testicular Anomalies in the Hybridogenetic Frog Pelophylax esculentus (Amphibia: Anura: Ranidae)” in The Second International conference “Amphibian and reptiles anomalies and pathology: methodology, evolutionary significance, monitoring and environmental health”, KnE Life Sciences. 2018. p. 92–96.
91. Kaiser J. A trematode parasite causes some frog deformities. 1999.
92. Fort DJ, Rogers RL, Bacon JP. Deformities in cane toad (Bufo marinus) populations in Bermuda. Part II. Progress towards characterization of chemical stressors. Applied Herpetology. 2006;3:143–172.
93. Savage AE, Becker CG, Zamudio KR. Linking genetic and environmental factors in amphibian disease risk. Evolutionary Applications. 2015;8(6):560–572.
94. Levey R, Shambaugh N, Fort D, et al. Investigations into the causes of amphibian malformations in the Lake Champlain Basin of New England. Waterbury, VT: Vermont Department of Environmental Conservation. 2003.
95. Ohler A, Dubois A. “Anomalies in natural populations of amphibians: Methodology for field studies” in The Second International conference “Amphibian and reptiles anomalies and pathology: methodology, evolutionary significance, monitoring and environmental health”. KnE Life Sciences. 2018;123–132.
96. Svinin AO, Bashinskiy IV, Litvinchuk SN, et al. Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs. Parasites and Vectors. 2020;13(1):1–11.
97. Johnson PT, Lunde KB, Thurman EM, et al. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs. 2002;72(2):151–168.
98. Pessier AP. An overview of amphibian skin disease. In Seminars in avian and exotic pet medicine. 2002;11(3):162–174.
99. Johnson PTJ, Reeves MK, Krest SK. A decade of deformities: advances in our understanding of amphibia n malformations and their implications. Ecotoxicology of amphibians and reptiles. 2010;2:511–536.
100. Hecker L, Sessions SK. Developmental analysis of limb deformities in amphibians. Bioscience. 2001;72(1):9–13.
101. Ankley GT, Diamond SA, Tietge JE, et al. Assessment of the risk of solar ultraviolet radiation to amphibians. I. Dose-dependent induction of hindlimb malformations in the northern leopard frog (Rana pipiens). Environmental Science and Technology. 2002;36(13):2853–2858.
102. Reeves MK, Jensen P, Dolph CL, et al. Multiple stressors and the cause of amphibian abnormalities. Ecological Monographs. 2010;80(3):423–440.
103. Kaiser J. Fifty years of deformed frogs. 2003.
104. Loeffler IK, Stocum DL, Fallon JF, et al. Leaping lopsided: a review of the current hypotheses regarding etiologies of limb malformations in frogs. The Anatomical Record: An Official Publication of the American Association of Anatomists. 2001;265(5):228–245.
105. McDevitt-Galles T, Carpenter SA, Koprivnikar J. How predator and parasite size interact to determine consumption of infectious stages. Oecologia. 2021;197(3):551–564.
106. Sessions SK, Franssen RA, Horner VL. Morphological clues from multilegged frogs: Are retinoids to blame? Science. 1999;284(5415):800–802.
107. Summers CG. Albinism: classification, clinical characteristics, and recent findings. Optometry and Vision Science. 2009;86(6):659–662.
108. Marco A, Quilchano C, Blaustein AR. Sensitivity to nitrate and nitrite in pond-breeding amphibians from the Pacific Northwest, USA. Environmental Toxicology and Chemistry. 1999;18:2836–2839.
109. Helgen JC, Gernes MC, kerten SM, et al. Field investigations of malformed frogs in Minnesota 1993–97. Journal of the Iowa Academy of Science. 2009;107:96–112.
110. Johnson PTJ, Lunde KB, Zelmer DA, et al. Limb Deformities as an Emerging Parasitic Disease in Amphibians: Evidence from Museum Specimens and Resurvey Data. Conservation Biology. 2003;17(6):1724–1737.
111. Mônico AT, Ferreira RB, Lauvers WD. Itapotihyla langsdorffii (Perereca Castanhola; Ocellated Treefrog): Head Abnormality. Herpetological Review. 2016;47(2):278–279.
112. Read JL, Tyler MJ. Natural levels of abnormalities in the trilling frog (Neobatrachus centralis) at the Olympic Dam mine. Bulletin of Environmental Contamination and Toxicology. 1994;53:25–31.
113. Rodríguez P, Fernández J. Effects of direct human disturbance on the endemic Iberian frog Rana iberica at individual and population levels. Biological Conservation. 2005;123(1):1–9.
114. Spolyarich N, Hyne R, Wilson S, et al. Morphological abnormalities in frogs from a rice-growing region in NSW, Australia, with investigations into pesticide exposure. Environmental monitoring and assessment. 2011;173(1–4):397–407.
115. Stebbins RC. A field guide to western reptiles and amphibians. Second edition. Houghton Mifflin Company, Boston, Massachusetts. 2000. p. 350.
116. Stocum DL. Invited editorial: frog limb deformities: an “eco-devo” riddle wrapped in multiple hypotheses surrounded by insufficient data. Teratology. 2000;62:147–150.