Vasconcelos-Filho et al., / Revista Brasileira de Higiene e Sanidade Animal (v.9, n.3) (2015) 386-399
Revista Brasileira de Higiene e Sanidade Animal
Brazilian Journal of Hygiene and Animal Sanity ISSN: 1981-2965
Natural history and biological aspects of dipsadidae snakes: P. olfersii, P. patagoniensis and P. nattereri
História natural e aspectos biológicos de serpentes dipsadidae: P. olfersii, P. patagoniensis e P. Artigo nattereri
Francisco Sérgio Lopes Vasconcelos-Filho1*, Roberta Cristina da Rocha-e-Silva2, Rebeca Horn Vasconcelos2, Joselito de Oliveira Neto2; João Alison de Moraes Silveira3, Glayciane Bezerra de Morais2, Nathalie Ommundsen Pessoa2, Janaina Serra Azul Monteiro Evangelista2
1 Laboratory of Biochemistry and Gene Expression – State University of Ceará. 2Laboratory of Histology of Effects Caused by Snake Venoms and Plants – State University of Ceará. 3Laboratory of Pharmacology of Venoms, Toxins and Lectins – Federal University of Ceará
ABSTRACT. Attacks by venomous snakes are a serious public health problem, accounting for 464 deaths from 2010 to 2013. However, this statistic does not seem to correspond with reality, as some poisonous snakes are not considered poisonous due to anatomic location of their fangs. The genus Philodryas belongs to the family Dipsadidae, comprising over 700 species. Philodryas olfersii, P. patagoniensis and P. nattereri, occur in the Caatinga biome and are characterized by diurnal habits, generalist diet and habitat. Although not considered poisonous, the Duvernoy's gland present in these reptiles produces toxic substances that act similar to B. jararaca and may cause local and systemic effects. Keywords: venom effect; biome; reproductive cycle; sexual dimorphism. RESUMO: Ataques por serpentes peçonhentas é um grave problema de saúde pública, sendo responsável por 464 óbitos de 2010 a 2013. No entanto esse número parece não corresponder com a realidade, já que algumas serpentes venenosas não são consideradas peçonhentas devido a localização anatômica de sua presa inoculadora. O gênero Philodryas pertence à família Dipsadidae, constituída por mais de 700 espécies. Philodryas olfersii, P. patagoniensis e P. nattereri, ocorrem na Caatinga e são caracterizadas por hábitos diurnos, dieta e habitat generalista. Embora consideradas não peçonhentas, a glândula de Duvernoy presente nesses répteis produz substâncias tóxicas com ação semelhante ao B. jararaca, podendo causar efeitos locais, e sistêmicos. Palavras-chave: efeito do veneno; bioma; ciclo reprodutivo; dimorfismo sexual. ______Recebido 07/07/2015; Aceito 15/09/2015 Author for Correspondence. Email: * [email protected] http://dx.doi.org/10.5935/1981-2965.20150036 386
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INTRODUCTION Philodryas genus consists of 20 species and
Envenomations represent a serious three of these are found in the Northeast public health problem and snakes are the most region of Brazil: P. olfersii, P. patagoniensis frequently responsible for these acidents. In and P. nattereri (UETZ, 2013). Although not
Brazil, 103,422 snakebites were registered considered venomous, studies show that the with 464 deaths between the years 2010 to Duvernoy's gland present in these reptiles
2013. In Ceará State, during the same period, produces toxic substances that act similar to
2,328 attacks were reported (SINAN, 2013). the venom of B. jararaca and may cause local
However, this number does not seem to and systemic effects (Prado-FRANCESCHI et correspond to reality, since some poisonous al., 1998; RIBEIRO et al., 1999; PEICHOTO snakes are not considered poisonous (LEMOS et al., 2006; ZELANIS et al., 2010). et al., 2009). However, few studies address the biological,
This is due to the morphological the natural history and the effects of this kind characteristics of the fangs, since venom, with most targeted species being P. opisthoglyphous snakes have difficulty in olfersii and P. patagoniensis due to the more injecting the venom due to the location of the frequent reports of attacks by these species, fangs in the back of the upper jaw, requiring a including a report of a fatality caused by P. longer period of bites to inject their venom olfersii (SALOMÃO AND DI-BERNARDO, into the prey, such as species of Dipsadidae 1995). Therefore, the present study aimed to family (MEDEIROS et al., 2010; MENEZES carry out a literature review about the biome, et al., 2013). reproductive cycle, sexual dimorphism and
The Dipsadidae family is one of the biological effect of the venoms of P. olfersii, largest families of Colubroides, consisting of P. patagoniensis and P. nattereri. more than 700 species, among them
Philodryas spp. (UETZ, 2013). The
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HABITAT, SEASON AND DAILY All species have similar seasonal ACTIVITY and daily foraging activity, varying the P. olfersii, P. nattereri and P. pattern of activity during the year. In rainy patagoniensis are found in the Caatinga months, the amount of active snakes is biome, but have different habitat behaviors higher, possibly due to the higher (RODRIGUES, 2003; SANTOS et al., 2008; availability of prey and to reproduction MESQUITA et al., 2013). P. olfersii is purposes. The daily activities of these described as semi-arboreal because it is snakes is exclusively diurnal, being more commonly found in soils and forests, concentrated in the warmer periods of the however, when in the woods, it is seen more day (HARTMANN AND MARQUES, often on vegetation. P. nattereri is a species 2005; PONTES, 2007; MESQUITA et al., with generalist habitat behaviors, performing 2011; MESQUITA et al., 2013). mainly terrestrial activity, although it is also FEEDING HABITS arboreal and fossorial (HARTMANN AND The feeding habits of Philodryas MARQUES, 2005; MESQUITA et al., 2012; spp. are quite diverse. Their diet consists MESQUITA et al., 2013). MESQUITA of: lizards, frogs, mammals, birds, fish and (2010) believes that these snakes also have squamata eggs. However, the preference significant fossorial activity. But it is difficult for certain prey varies according to the to prove this behavior because of the species. P. olfersii has greater interest in difficulties in checking underground frogs (HARTMANN AND MARQUES, environments effectively. In contrast, some 2005 FRANCE et al., 2008; MESQUITA researchers claim that this species should be et al., 2013), although it is common to prey characterized only as terrestrial (VITT, 1980; on passerines (CARVALHO AND VITT AND VANGILDER, 1983; NOGUEIRA, 1998; HARTMANN AND CARVALHO AND NOGUEIRA, 1998; MARQUES, 2005; OUTEIRAL, 2005; Costa, 2006). P. patagoniensis seems to be FRANÇA et al., 2008; ALMEIDA AND mainly terrestrial, although also perform SANTOS, 2011). arboreal activity to prey (HARTMANN AND Nevertheless, BALESTRIN (2008) MARQUES, 2005; PONTES, 2007). found in a study conducted in a sierra in Ontological differences in habitat use can also Southeast of Rio Grande do Sul, that the diet be identified and may be related to survival. of this snake was exclusively composed of Juveniles are mostly found in open areas birds. Although the birds are also part of P. (CARVALHO AND NOGUEIRA, 1998; patagoniensis diet and P. nattereri, this type PONTES, 2007). of animal is more frequently preyed upon by
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P. olfersii, possibly because this species use HARTMANN et al., 2009; MESQUITA more arboreal substrate than the others do. P. AND BORGES-NOJOSA, 2009; nattereri displays preference for diets based MESQUITA et al., 2011.). on lizards, but squamata eggs and snakes are This variation is influenced by the also a part of their diet (CARVALHO AND size of the snake, since juveniles have NOGUEIRA, 1998; MESQUITA AND difficulty to subdue large prey and the BORGES-NOJOSA, 2009; MESQUITA et availability associated with the use of al., 2010; MESQUITA et al., 2011; microhabitat, which explains the higher GODINHO et al., 2012; MESQUITA et al., incidence of birds in P. olfersii diet 2013). Intake of squamata eggs is more likely (PONTES, 2007). SAZIMA AND MARTINS to happen among snakes that also prey on (1990) observed that young snakes tend to those adult squamata species (QUEIROZ perform large prey attacks, however, because AND RODRIGUEZ-ROBLES, 2006). P. the size of prey these snakes are forced to patagoniensis are interested in frogs, but it is regurgitate them and seek smaller prey. common to verify the occurrence of snakes of MENEZES AND COLLEAGUES (2013) the same species in their diet. P. reported the death of P. nattereri after patagoniensis is possibly the only one of the ingesting of a large lizard of the species three species with cannibalistic habits Tropidurus hispidus. The authors suggested (LÓPEZ, 2003; HARTMANN AND that the size of the lizard exerted pressure on MARQUES, 2005; OLIVEIRA, 2005; internal organs hindering lung mechanics, HARTMANN et al., 2009; PONTES, 2007). resulting in asphyxiation. Moreover, the extra Conspecific predation is a common weight of ingested prey may have affected the event in several families of snakes (Boidae, mobility of the snake, overextending the time Colubridae, Elapidae and Dipsadidae) and spent the substrate, leading to hyperthermia apparently is related to snakes with generalist followed by dehydration. and ophiophagous diet (LOURDAIS et al., REPRODUCTION AND DIMORPHISM 2004; HARTMANN AND MARQUES, Snake reproduction is closely related to 2005; FREIRÍA et al., 2006; PONTES, 2007; the fertile period of females. This period is GÖÇMEN et al., 2008; Hartmann et al., characterized by the presence of follicles in 2009). Quantitative (number of different secondary vitellogenesis and eggs in the items consumed) and qualitative (types of oviduct or folded oviducts, indicating recent items consumed) ontogenetic variation can be oviposition (SHINE, 1978). The males are observed in these species (HARTMANN considered mature when the testicles are AND MARQUES, 2005; PONTES, 2007;
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Vasconcelos-Filho et al., / Revista Brasileira de Higiene e Sanidade Animal (v.9, n.3) (2015) 386-399 turgid and vas deferens are compressed olfersii (FOWLER AND SALOMÃO, (SHINE, 1980; SLIP AND SHINE, 1988). 1994; MESQUITA et al., 2013). These According to LÓPEZ AND GIRAUDO characteristics can be directly related to the (2008) the reproductive period of Philodryas reproductive cycle, since larger females patagoniensis females is seasonal. The have the capacity to produce more eggs authors noted that this species has vitellogenic and larger tails accommodate better the period between July and October. However, hemipenis of males and facilitate BALESTRIN (2008) found that the fertile intercourse (BALESTRIN, 2008; LOPEZ period of this Dipsadidae is longer presenting AND GIRAUDO, 2008; MESQUITA et follicles between the months of October to al., 2011; MESQUITA et al., 2013). The March. The reproductive cycle of P. olfersii is absence of dimorphism between males and long and occurs between the months of females concerning the size of the head is October to April (BALESTRIN, 2008) or related to food niche, since each sex can between June-December (MESQUITA et al., prey on different types or sizes. Therefore, 2011). MESQUITA et al. (2013) reported the this lack of dimorphism suggests that both presence of vitelogenic follicles in P. olfersii sexes feed on similar prey (MESQUITA et throughout the year. Although females al., 2011). present vitelogenic follicles throughout the BIOLOGICAL VENOM EFFECTS year, the reproductive cycle of this snake is Snake venoms are complex not continuous because ovulation is clearly mixtures of protein and non-protein seasonal and restricted to November-January. components which have a wide range of Moreover, males apparently have a period of biological activities (ZELANIS et al., reproductive dormancy during the colder 2010). Nevertheless, these components months (June to September). P. nattereri, like have been widely studied in order to the other species, has a long reproductive determine these bioactive compounds and cycle ranging between February and October, their possible therapeutic potential. indicating a prolonged breeding season that However, these studies seek substances was not influenced by seasonality that can be used in the production of (MESQUITA et al., 2011). pharmaceuticals for treating various All species show similar sexual chronic diseases such as hypertension, dimorphism. Females have snout-vent diabetes mellitus, cancer, etc. Some length greater than males, but the latter authors have observed the effect of have relatively longer tails. This Crotalus durissus cascavella, Bothrops difference, however, does not occur in P. jararaca and Naja naja atra venoms, and
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Vasconcelos-Filho et al., / Revista Brasileira de Higiene e Sanidade Animal (v.9, n.3) (2015) 386-399 the possible pharmacological potentials, limb, and forming two areas of bruises. by observing arterial hypotension, the This edema lasted for 15 days and systemic increase in nitric oxide production, reduced effects were not identified. hyperglycemia and cytotoxicity in tumor Moreover, PEICHOTO, cells, inducing them to necrosis and/or CÉSPEDEZ AND PASCUAL (2007) apoptosis, respectively (EVANGELISTA observed the presence of burning pain after et al., 2011; JORGE et al, 2011; NUNES the bite of P. olfersii as well as severe et al., 2012). Although Philodryas spp. vertigo, nausea and vomiting which lasted venom has a similar effect to the venom of for two weeks even after drug intervention Bothrops spp. there are only a few studies in the patient. The presence of transient concerning the biological effects of bleeding, erythema, as well as the clinical Philodryas spp. venom (ACOSTA et al., signs already mentioned above have been 2003; PEICHOTO et al., 2005; ROCHA reported but not affecting all cases AND FURTADO, 2007). diagnosed as P. olfersii attacks (RIBEIRO After inoculating the venom of a et al., 1999). In contrast, bruising after the species of the family Dipsadidae, the attack of P. patagoniensis is not observed following signs can be observed in the (MEDEIROS et al., 2010). victim: Pain, swelling, bruising, transient The secretion of P. patagoniensis bleeding, muscle necrosis and systemic Duvernoy's gland displays biologically effects such as dizziness and vomiting intense edema activity and the increase of (ASSAKURA et al., 1992; Prado- this activity is directly proportional to the FRANCESCHI et al., 1996; 1998; amount of venom in the inoculated animal, ARAÚJO AND SANTOS, 1997; being the minimum dose of edema RIBEIRO et al., 1999; PEICHOTO et al., identified 0.26 µg/mice (PEICHOTO et al., 2007A; PEICHOTO et al., 2007B; COSTA 2004). ROCHA AND FURTADO (2007) et al., 2008; MEDEIROS et al., 2010; showed that edema effect of P. olfersii and ZELANIS et al., 2010). ARAÚJO AND P. patagoniensis venoms was very rapid, SANTOS (1997) reported that the bite of occurring between 5 and 10 minutes after Philodryas olfersii and P. patagoniensis inoculation, reaching the maximum effect did not cause immediate pain or bleeding. within 30 min and remained stable until the However, 15 minutes after the accident, fourth hour after envenomation. edema onset was observed that later Some studies showed that the progressed to the forearm and arm venom from the Duvernoy's gland of P. hindering the movement of the affected patagoniensis (ACOSTA et al., 2003;
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PEICHOTO et al., 2005; ROCHA AND increasing the intensity over time (Prado- FURTADO, 2007) and P. olfersii Franceschi et al., 1996; 1998; Acosta et al. (ROCHA AND FURTADO, 2007) have 2003; PEICHOTO et al., 2007B). ROCHA high hemorrhagic activity, peaking activity AND FURTADO (2007) proposed from two to four hours, and minimal minimum necrotizing doses between 79.1 bleeding doses of 24μg/mouse for P. and 63.5μg/mouse for P. olfersii venom olfersii venom and 26.9μg/mouse for P. and P. patagoniensis venom, respectively. patagoniensis venom (ROCHA AND This necrosis is possibly caused by FURTADO, 2007). These data are similar the proteolytic enzymes present in the to results obtained in other studies that venom that degrade the extracellular found a minimum bleeding dose of matrix of tissues. This can be seen more 0.5μg/mouse for P. olfersii venom prominently on the outskirts of the (ASSAKURA et al., 1992) and gastrocnemius muscle inoculated with the 0.27μg/mouse for P. patagoniensis venom venom, where there was degradation of (PEICHOTO et al., 2007B). The myofibrils, damaging and inhibiting hemorrhagic activity was probably caused muscle contractions, (PRADO- by metalloproteinases that degrade the FRANCESCHI et al., 1998). Another secretion of basement membrane proteins factor in the diagnosis of myonecrosis was from the blood vessel wall, resulting in a increased creatine kinase (CK) in plasma, loss of capillary integrity, thus leading to a which is a specific marker for muscle local bleeding. Furthermore, the damage (PRADO-FRANCESCHI et al., fibrinogenolytic enzymes reduce plasma 1998; PEICHOTO et al., 2004). The fibrinogen by hydrolysis hindering the Duvernoy's gland secretion of P. coagulation (ACOSTA et al., 2003; patagoniensis also presented PEICHOTO et al., 2005). dermonecrotic activity when tested by Philodryas spp. venom have high intradermal method in rodents, showing an proteolytic activity, surpassing even intense effect (15.7μg/mouse), Bothrops alternatus venom (GAY et al., demonstrated by the presence of 2005) and B. jararaca venom (ROCHA et degeneration of the epidermis and signs of al., 2006). This appears to a determining necrosis in the dermis, which was factor, resulting in extensive myonecrosis, accompanied by an inflammatory infiltrate characterized by the presence of pyknotic (PEICHOTO et al., 2004). nuclei - condensation of nuclear chromatin Little is known about the biological (PRADO-FRANCESCHI et al., 1998), effects of the P. nattereri venom.
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ZELANIS et al. (2010) conducted a study diet, and preferably frogs or lizards as about biochemical characterization of the main preys. Their reproductive cycle, Philodryas spp. venom and showed that although uncertain, seems long for P. the secretion of P. nattereri has a nattereri and seasonal for the other two composition similar to the P. olfersii and species. Like other snakes, these P. patagoniensis venoms with high Dipsadidae members are characterized by proteolytic action, but with discrete females larger than males, but the latter fibrinogenolytic activity. The authors also have longer tails. The biological effects reported the presence of phospholipase A2 from the venoms of these snakes was activity in this genus. shown to have potent edema, hemorrhage, The use of chelating substances as well as myo and dermonecrotic, effects have been reported to decrease or inhibit often comparable with Bothrops sp venom. the effects of metalloproteinases present in Dessa forma, outros estudos devem the venom such as EDTA (ASSAKURA et ser realizados a fim de se obter mais al., 1992; ACOSTA et al., 2003; Rocha et conhecimento acerca dessas espécies, al., 2006) and the association of Na2EDTA referente aos efeitos sistêmicos do veneno and Benzamidine (PEICHOTO et al., de Philodryas, especialmente P.nattereri,
2005) or Na2EDTA and DTT (PEICHOTO devido à escassez de informações na et al., 2007B), respectively. The pH change literatura. Portanto, a importância de se also shows a decrease in activity at acidic estudar e verificar os possíveis efeitos pH (ASSAKURA et al., 1992; PEICHOTO morfofisiológicos e terapêuticos dos et al., 2007B) and basic pH (PEICHOTO et componentes do veneno dessas espécies, al., 2007B). Therefore, the use of these torna-se de grande relevância para a substances to reduce or inhibit the comunidade científica, na busca de hemorrhagic, necrotizing and edema substâncias com potencial activities of the Philodryas spp. venom is fisiofarmacológico. proposed. Thus, further studies should be CONCLUSIONS performed in order to obtain more Therefore, according to the knowledge about these species, targeting information shown, the snakes of the genus the systemic effects of Philodryas venom, Philodryas spp. have generalist habits and especially P. nattereri due to lack of may be categorized as terrestrial, arboreal information in the scientific literature. and fossorial. Furthermore, this genus has Therefore, the importance of studying and a wide variety of small animals in their verifying the morphophysiological and
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Vasconcelos-Filho et al., / Revista Brasileira de Higiene e Sanidade Animal (v.9, n.3) (2015) 386-399 therapeutic effects of venom components snake). Toxicon, v. 30, n. 4, p. 427-438, of these species is of great relevance to the 1992. scientific community in the search for BALESTRIN, R.L.S. História natural de substances with physio-pharmacological uma taxocenose de squamata e redescrição potential. de uma espécie de anuro no escudo Sul- REFERENCES Riograndense, Brasil, 2008. 148p. Tese ACOSTA, O.; LEIVA L.C.; PEICHOTO (doutorado em Zoologia). Pontifícia M.E.; MARUÑAK S.; TEIBLER P.; REY Universidade do Rio Grande do Sul, 2008. L. Hemorrhagic activity of the Duvernoy's CARVALHO, M.A.; NOGUEIRA F. gland secretion of the xenodontine colubrid Serpentes da área urbana de Cuiabá, Mato Philodryas patagoniensis from the north- Grosso: aspectos ecológicos e acidentes east region of Argentina. Toxicon, 41(8), ofídicos associados Snakes from the urban 1007-1012, 2003. area of Cuiabá, Mato Grosso: ecological ALMEIDA G.V.L.; SANTOS E.M. Nota aspects and. Caderno de Saúde Pública, sobre predação de Passer domesticus v. 14, n. 4, p. 753-763, 1998. (Aves, Passeridae) por Philodryas olfersii COSTA, T. Estrutura da comunidade de (Squamata, Dipsadidae) em uma área Serpentes de uma área de Caatinga do urbana na Zona da Mata de Pernambuco, Nordeste brasileiro, 2006. 74 pp. Brasil. Boletim do Museu Paraense Dissertação (Mestrado em Ciências Emílio Goeldi., v. 6, n. 3, p. 351-354, Biológicas), Universidade Federal do Rio 2011. Grande do Norte, RN, 2006. ARAÚJO M.E.; SANTOS A.C.M.C.A. EVANGELISTA, J.S.A.M.; Cases of human envenoming caused by EVAGELISTA, J.J.F.; EVANGELISTA, Philodryas olfersii and Philodryas I.L.; NOJOSA, D.M.B.; NASCIMENTOS patagoniensis (Serpentes: N.R.F.; SOUZA M.H.L.P.; ALVES R.S.; Colubridae). Revista da Sociedade MARTINS A.M.C.; MORAES M.E.A.; Brasileira de Medicina Tropical, v. 30, n. MONTEIRO H.S.A. Hypotensive effects 6, p. 517-519, 1997. of the Crotalus durissus cascavella venom: ASSAKURA M.T.; SALOMÃO M.G.; involvement of NO. Natural product PUORTO G.; MANDELBAUMI F.R. communications, v. 6, n. 6, p. 871, 2011. Hemorrhagic, fibrinogenolytic and edema- FOWLER, I.R.; SALOMÃO, M.G. A forming activities of the venom of the study fo sexual dimorphismin six species colubrid snake Philodryas olfersii (green from the colubrid snake genus Philodryas. The snake. v. 26, p. 117-122, 1994.
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