Opossums (Mammalia: Didelphidae) in the diets of Neotropical pitvipers (Serpentes: Crotalinae): Evidence for alternative coevolutionary outcomes?

Toxicon 66 (2013) 1–6

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Opossums (Mammalia: Didelphidae) in the diets of Neotropical pitvipers (Serpentes: Crotalinae): Evidence for alternative coevolutionary outcomes? Robert S. Voss Division of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 October 2012 Received in revised form 2 January 2013 Accepted 15 January 2013 Available online 8 February 2013

Opossums and pitvipers are sympatric throughout most of the New World, but trophic relationships between these speciose clades have only recently attracted the attention of researchers. Although it is now known that some venom-resistant opossums prey on pitvipers, a review of the literature on diets shows that some Neotropical pitvipers prey on opossums. Interestingly, some pitviper species prey on opossums known or suspected to be venom resistant. If venom resistance and venom potency are coevolved traits, then these observations suggest that alternative outcomes may result in role-switching between victims and exploiters. Because molecular antagonists (e.g., venom toxins and toxinneutralizing serum proteins) that could mediate such outcomes have been plausibly identified, this system is a potentially fruitful field for evolutionary research. Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Arms race Bothrops Coevolution Predation Venom

“Sería igualmente interesante estudiar otros géneros de Didelphidae sud-americanos, a fin de averiguar si se trata de inmunidad propia a todo el grupo o limitada a las mayores especies, que deben ser las únicas capaces de atacar a las serpientes venenosas” (Vellard, 1949: 31). [It would be equally interesting to study other South American didelphid genera to determine whether immunity is a group trait, or if it is limited to the larger species, which are probably the only ones capable of attacking venomous snakes.]

1. Introduction Although opossums and pitvipers are sympatric throughout most of the New World, trophic interactions between members of these clades were long unsuspected. Vellard (1945, 1949), however, discovered that three South E-mail address: [email protected]. 0041-0101/$ – see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.toxicon.2013.01.013

American species of Didelphis are resistant to the venom of several pitviper species, from which they are protected (in part) by endogenous toxin-neutralizing serum proteins. Vellard proposed that venom resistance in Didelphis evolved as an adaptation for preying on venomous snakes, but he also implied (in the passage quoted above) that this hypothesis might be falsified if other opossums, too small to eat venomous snakes, were also found to be venom resistant. Subsequent researchers (e.g., Werner and Vick, 1977; Perales et al., 1994) reported venom resistance in the North American opossum (Didelphis virginiana), the lutrine opossum (Lutreolina crassicaudata), and the gray “four-eyed” opossum (Philander frenatus). To date, all of the opossum species found to be venom resistant belong to the tribe Didelphini (sensu Voss and Jansa, 2009, Table 1), all are relatively large (>ca. 500 g mean adult weight), and several are known to eat venomous snakes (Jansa and Voss, 2011; Voss and Jansa, 2012). By contrast, experiments have shown that the brown four-eyed opossum (Metachirus nudicaudatus)da smaller (ca. 300–400 g) insectivorous

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Table 1 Resistance of didelphids to New World pitviper venoms. Only positive outcomes of in vivo challenges (indicated by survival of test animals following experimental snakebite and/or injection with a measured dose of venom judged to be lethal if administered to a nonresistant species of equivalent weight) are tabulated. Taxon challenged

Venom origin

Reference(s)

Didelphis albiventris

Bothrops spp.a, Crotalus durissus, Lachesis muta Crotalus durissus Bothrops spp.a, Crotalus durissus, Lachesis muta Bothrops jararaca Bothrops spp.a, Crotalus durissus, Lachesis muta Bothrops jararaca, Crotalus adamanteus, C. durissus Bothrops asper and/or B. venezuelensis Crotalus spp.b, Agkistrodon spp.c

Vellard (1945, 1949)

Didelphis aurita

Didelphis marsupialis

Didelphis virginiana

Lutreolina crassicaudata Philander frenatus a b c

Farah et al. (1996) Vellard (1945, 1949) Perales et al. (1994) Vellard (1945, 1949) Moussatché et al. (1978, 1979) Pifano et al. (1993)

Bothrops jararaca

Kilmon (1976), Werner and Vick (1977) Perales et al. (1994)

Bothrops jararaca

Perales et al. (1994)

Bothrops alternatus, B. jararaca, and B. neuweidii. Crotalus adamanteus, C. atrox, and C. horridus. Agkistrodon bilineata, A. contortrix, and A. piscivorus.

speciesdis not venom resistant (Perales et al., 1994). Although these facts are obviously consistent with Vellard’s hypothesis that venom resistance evolved as a predatory adaptation, much remains to be learned about trophic relationships between opossums and pitvipers. The exceptionally rapid evolution of snake-venom toxins has prompted some researchers to suggest that venomous snakes are in a biochemical arms race with their prey (Gibbs and Rossiter, 2008; Juárez et al., 2008; Mackessy, 2010), but the recent discovery of accelerated evolution in a venom-targeted blood protein among didelphid species known to eat pitvipers suggests that these snakes may additionally (or instead) be in an arms race with their predators (Jansa and Voss, 2011). Much experimental evidence obtained in recent decades (reviewed by Voss and Jansa, 2012) has confirmed and extended Vellard’s discovery that some opossums have evolved impressive resistance to pitviper venom, but opossums and pitvipers are taxonomically diverse groups between which numerous pairwise coevolutionary interactions with various outcomes are possible. Conceivably, pitvipers are not always the hapless prey of venomresistant opossums. If the arms-race scenario is appropriate, ophiophagous opossums may have “won” some coevolutionary contests, but not others. Knowing who eats whom is key for understanding the ecological context in which venom resistance and venom potency may have coevolved. Predation events in the wild are seldom witnessed by researchers, so relevant data tend to be anecdotal and widely dispersed in the literature. Records of opossum predation on pitvipers were reviewed by Voss and Jansa (2012), but records of pitviper predation on opossums have not previously been reviewed. Pitvipers normally ambush live prey, which they subdue by envenomation, although scavenging is known to occur

in some species (DeVault and Krochmal, 2002). Typically, pitvipers release mammalian prey after a lightning-fast stabbing bite and then wait for the stricken victim to stagger off and die before tracking and eating it (Cundall, 2002; Deufel and Cundall, 2006). Therefore, in the absence of fly larvae or other indication of scavenging, the discovery of an opossum in a pitviper’s digestive tract or feces is prima facie evidence that the species in question is not resistant to the venom of the snake that ate it. To gain understanding about the natural history of predatory interactions between opossums and pitvipers, I surveyed the literature for published records of snake-onopossum predation events. Additionally, I examined preserved prey items in herpetological collections and analyzed scat samples of wild-collected snakes donated by herpetologists. Although the resulting data are not extensive, they suggest the existence of diverse trophic relationships that merit the attention of both field biologists and experimental researchers. 2. Results 2.1. Published records of didelphids in pitviper diets Unidentified opossums have been reported as prey of at least ten Neotropical pitviper species (Table 2). These records include unvouchered observations of “opossums”, “marsupials”, “cuicas”, etc. in the diets of snakes from regions where two or more didelphid species are known to occur (e.g., Honduras; March, 1928), as well as reports based on obsolete taxonomic usage that cannot be definitely associated with modern taxa. An example of the latter is “Marmosa” as used by da Cunha and do Nascimento (1978), which could refer to species in any of several didelphid genera currently recognized in the area where they worked (e.g., Gracilinanus, Marmosa sensu stricto, or Marmosops). Although such indefinite records are useless for scoring the phylogenetic distribution of venom resistance, they serve to establish that didelphids are, in fact, eaten by a wide range of Central and South American pitvipers. Of greater interest are positive identifications of didelphids from the digestive tracts and/or scat of eleven Neotropical pitviper species (Table 3). Most of the publications reporting these records were authored (or co-authored) by Table 2 Published records of pitviper predation on unidentified opossums. Pitviper species

Locality

Reference

Bothrops Bothrops Bothrops Bothrops

S Brazil Costa Rica Honduras N Brazil

Nunes et al. (2010) Picado (1976) March (1928) da Cunha and do Nascimento (1978) da Cunha and do Nascimento (1978) Hartmann et al. (2005) March (1928) Dixon and Soini (1986) Campbell and Lamar (2004) Sant’Anna and Abe (2007) Solórzano (2004) Solórzano (2004)

alternatus asper asper atrox

Bothrops brazili

N Brazil

Bothrops pubescens Bothriechis schlegelii Bothriopsis taeniata Bothriopsis taeniata Crotalus durissus Lachesis melanocephala Lachesis stenophrys

S Brazil Honduras NE Peru SE Peru SE Brazil Costa Rica Costa Rica

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Table 3 Positive identifications of didelphids eaten by pitvipers. Species marked with an asterisk are known to be resistant to pitviper venom or are closely related to venom-resistant species. Opossum species

Pitviper species

Location

Reference

Caluromys derbianus Caluromys philander Caluromys philander Didelphis marsupialis* Didelphis marsupialis* Didelphis marsupialis*

Bothrops asper

Costa Rica

Hirth (1964)

Bothrops asper

Trinidad

Mole (1924)

Bothrops jararaca Bothrops asper

SE Brazil

Lira et al. (2007)

Costa Rica

Greene (1989)

Bothrops asper

Costa Rica

This study

Bothrops lanceolatusa

Martinique

Gracilinanus agilis Marmosa macrotarsus Marmosa mexicana Marmosa waterhousei Marmosops caucae Marmosops noctivagus Metachirus nudicaudatus Monodelphis brevicaudata Monodelphis emiliae Philander opossum* Philander opossum* Philander opossum*

Bothrops pauloensis Bothrops atrox

SE Brazil

Henderson and Powell (2009), this study Valdujo et al. (2002) This studyb

Crotalus durissus

Costa

Bothrops atrox

NE Peru

Bothriechis schlegelii Bothrocophias microphthalmus Bothrops jararacussu Lachesis muta

Colombia

Bothriopsis taeniata Bothrops asper

NE Peru

Bothrops asper

Guatemala

Lachesis muta

French Guiana

a b c

NE Peru

Ecuador Brazil N Brazil

Costa Rica

Rica Allen (1891) This studyc Gertler and Morales (1980) Cisneros-Heredia et al. (2006) Lanschi et al. (2012) Martins and Oliveira (2002) Pitman et al. (2003) Sasa et al. (2009), this study Campbell (1998; pers. com.) Atramentowicz (1986)

Originally reported as Bothrops caribbaeus (see text). Prey dissected from AMNH R-54599. Prey dissected from AMNH R-54863.

herpetologists, so snake identificationsdherein updated to conform with taxonomic usage in Campbell and Lamar (2004)dare assumed to be accurate. The three published records of Caluromys are probably accurate because woolly opossums are easily identified by external characters (Emmons, 1997; Reid, 1997). Additionally, the Brazilian record of Caluromys philander eaten by Bothrops jararaca was based on an opossum radio-collared by mammalogists for an ecological study (Carlos et al., 2005; Lira et al., 2007). Species of Monodelphis are also morphologically distinctive, and both published records of this genus in pitviper diets are nonproblematic; the NE Peruvian record is, additionally, vouchered by a photograph (Fig. 1). The remains of Gracilinanus agilis in the diet of Bothrops pauloensis were identified by a mammalogist, and this record also seems reliable. The recent record of Metachirus from the stomach of Bothrops jararacussu is convincingly documented by a published photograph (Lanschi et al., 2012: Fig. 1). Both published records of Marmosops are vouchered by preserved specimens, but I was not able to examine either for this report.

Fig. 1. Bothriopsis taeniata eating Monodelphis emiliae, a predation event witnessed by Roosevelt García and Nigel Pitman at Quebrada Curacinha (5 030 S, 72 440 W; Pitman et al., 2003), Loreto, Peru (photo courtesy of Roosevelt García).

Two Marmosa records are based on my identifications of relatively intact material preserved as stomach contents in the AMNH herpetological collection, and the third was published by a mammalian taxonomist (Allen, 1891). All of the species discussed in the preceding paragraph are small (<500 g adult weight), none are known to eat snakes, and none belong to genera known to be venom resistant. By contrast, there are several records of pitviper predation on large opossums known to be venom-resistant, or that belong to genera with venom-resistant species. Each of these seemingly anomalous observations merits close scrutiny. Greene (1989: 1036) reported that Bothrops asper “take prey up to the size of opossums (Didelphis marsupialis)”. According to the author (H.W. Greene, pers. com., 2011), this statement was based on an observation by the American entomologist P.J. DeVries, who later told me (pers. com., 2011) that he had removed a large female opossum with nursing young from the stomach of a 1.5 m B. asper at La Selva, Costa Rica, in 1979 or 1980. Although DeVries thought that the opossum was D. marsupialis, he could not positively rule out alternative identifications, and no voucher specimen was preserved. However, he recalled that the animal made a bulge “the size of a football” (an American football is a prolate spheroid about 17
28 cm), that it had grayish fur, that the young were contained in a pouch, and that it could not have been Chironectes (which has externally obvious diagnostic features; Emmons, 1997;

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Reid, 1997). Given the locality where this observation was made, the only plausible identifications of DeVries’s opossum are D. marsupialis or Philander opossum. A scat sample of B. asper that I examined from a different Costa Rican locality contained the fur and teeth of D. marsupialis, lending credibility to DeVries’s original identification of this species in the La Selva snake, and captive B. asper have also been observed to kill and eat D. marsupialis (M. Sasa, pers. com., 2012). Campbell (1998) reported Philander in the diet of B. asper, apparently based on a specimen collected in Guatemala (J.A. Campbell, pers. com., 2012). Although I was not able to locate any voucher material, the record is plausible because P. opossum is the only opossum with pale supraocular spots (a key external character) known from the region encompassed by Campbell’s book (northern Guatemala, the Yucatan, and Belize). Additionally, Sasa et al. (2009) reported P. opossum from the diet of B. asper in Costa Rica, and I examined a Costa Rican scat sample of B. asper that contained fur and craniodental fragments of an adult P. opossum. Henderson and Powell (2009: 390) reported D. marsupialis in the diet of Bothrops caribbaeus, but the published snake identification was a lapsus for Bothrops lanceolatus (R.W. Henderson, pers. com., 2011). I was able to examine the prey voucher, which was recovered from the stomach of a large (snout-vent length ¼ 1557 mm) B. lanceolatus in the Museum of Comparative Zoology (MCZ R-75837). Despite being partially digested, the specimen is unquestionably a juvenile D. marsupialis. 2.2. Unconfirmed reports Murphy (1997) and Campbell and Lamar (2004) alleged that Mole (1924) reported D. marsupialis in the diet of B. asper from Trinidad, but this record appears to have been based on a nomenclatural misunderstanding. In fact, the opossum that Mole reported to have been eaten by B. asper (“Bothrops atrox” sensu lato) was Caluromys philander (“Didelphys philander” sensu lato), one of two didelphid species locally known as the “manicou gros yeux”. Sasa et al.’s (2009) inclusion of D. marsupialis in the diet of Trinidadian B. asper was based on Mole (1924) and Murphy (1997) and is, therefore, also invalid. Campbell and Lamar (2004: 348) cited Lazell (1964) to the effect that B. caribbaeus and B. lanceolatus (endemic to Saint Lucia and Martinique, respectively) eat Didelphis, but Lazell said nothing about opossums in the diet of B. caribbaeus and only remarked that B. lanceolatus was “reported” to eat Didelphis (presumably by locals). Although there is at least one valid record of B. lanceolatus predation on D. marsupialis (see above), there appears to be no valid record of opossums in the diet of B. caribbaeus; according to Schwartz and Henderson (1991), the only mammals known to be eaten by B. caribbaeus are introduced species of Mus and Rattus. 3. Discussion Most published accounts of New World pitviper diets concern temperate North American species of Agkistrodon

(moccasins and copperheads) and Crotalus (rattlesnakes). These snakes, although broadly sympatric with the Virginia opossum (D. virginiana) are not known to eat it. To be sure, adult Virginia opossums (which often weigh two to three kilograms; Gardner, 1982) are much too large to be swallowed by any but the very largest rattlesnakes. Young D. virginiana, however, are weaned and become independent when they are only 150–200 g, well within the size range of prey commonly eaten by A. piscivorus (water moccasin), Crotalus adamanteus (eastern diamondback rattlesnake), Crotalus atrox (western diamondback rattlesnake), and Crotalus horridus (timber rattlesnake). The absence of any published account of juvenile D. virginiana in the diets of these snakes is noteworthy given the extensive literature (reviewed by Klauber, 1972; Beavers, 1976; Clark, 2002; Campbell and Lamar, 2004) that might be expected to contain such records. By contrast, the much smaller literature on Neotropical pitviper diets includes multiple records of predation on opossums. Consistent with Vellard’s (1945, 1949) hypothesis that venom resistance is an evolved adaptation of large ophiophagous opossums, most positively identified didelphids recovered from pitviper digestive tracts are small (<500 g) species that are not known to eat snakes. However, published dietary data suggest that even venomresistant opossums may be vulnerable to predation by some pitviper species. In effect, the data reviewed here and elsewhere (Voss and Jansa, 2012) suggest that trophic relationships between opossums and pitvipers include at least three phenomena: (1) some pitvipers are preyed upon by large venom-resistant opossums; (2) many small opossums that are not known to be venom-resistant are preyed upon by pitvipers; and (3) venom-resistant opossums are preyed upon by some large pitvipers. The third category, previously unrecognized in the literature, could have two explanations. First, it seems probable that the efficacy of venom resistance in opossums is at least partially a function of blood volume. Of the two known mechanisms of snakevenom resistance in didelphidsdtoxin-neutralizing serum proteins and adaptive changes in substrate/ligand molecules (Jansa and Voss, 2011; Voss and Jansa, 2012)d the first seems likely to be overwhelmed if young individuals of venom-resistant species are bitten by large snakes. A relevant example might be the unique record of a juvenile D. marsupialis in the digestive tract of a 1.5 m specimen of B. lanceolatus (see above). Another record that might be explained in this context, of Philander opossum eaten by Lachesis muta, was not accompanied by information about the age of the opossum or the size of the snake, although L. muta (to 3 m) is among the largest of living pitvipers. Alternatively (or additionally), some pitvipers may have evolved unusually potent venom, possibly as a result of coevolution with venom-resistant predatory opossums. Possible examples of this outcome are several records of large opossums eaten by B. asper. Observations compiled in this review suggest that this species preys on adult D. marsupialis and Philander opossum, despite the fact that both opossums belong to a venom-resistant clade (Jansa and Voss, 2011), and that D. marsupialis itself is known to

R.S. Voss / Toxicon 66 (2013) 1–6

be highly resistant to the venom of other New World pitvipers (Table 1). There is also independent evidence that B. asper has exceptionally potent venom: laboratory experiments indicate that a toxin-neutralizing factor purified from the serum of Didelphis aurita (a species closely related to D. marsupialis) is less effective against the venom of B. asper than it is against any other New World pitviper venom tested (Neves-Ferreira et al., 1997). If an arms-race (sensu Dawkins and Krebs, 1979) is appropriate for conceptualizing the coevolution of venom resistance and venom potency in this system, then relevant molecular research might profitably focus on opossumpitviper species pairs in which exploiter-victim roles seem to be reversed. In particular, D. marsupialis/B. asper and D. aurita/B. jararaca. Whereas evidence summarized above suggests that Central American D. marsupialis is not resistant to the venom of sympatric B. asper, there is unequivocal experimental evidence (Perales et al., 1994) that Brazilian D. aurita is highly resistant to the venom of sympatric B. jararaca. Jararhagin and botrocetin, two potently hemorrhagic toxins in B. jararaca venom, have been extensively studied (e.g., by Paine et al., 1992; Usami et al., 1993; Fukuda et al., 2005; Moura-da-Silva and Baldo, 2012) and the molecular mechanisms by which their pathological effects are neutralized by venomresistant opossums are at least partially understood (Neves-Ferreira et al., 2000, 2002; Jansa and Voss, 2011). Probable homologs of jararhagin and botrocetin have been identified in B. asper venom (Angulo and Lamonte, 2009), but their physiological activity in sympatric D. marsupialis is unknown. Biochemically mediated role-switching between victims and exploiters is unusual (I am not aware of any other vertebrate example) and would seem to offer unique opportunities for insightful coevolutionary research. Of key importance for future progress in this field, however, is better information about the natural history of predatory interactions. As the preceding discussion makes clear, reliable taxonomic identifications are important in this context, as is information about the relative sizes of predator and prey individuals. Because chance observations of predation necessarily accrue slowly, it is important that each be reported accurately and in as much relevant detail as possible. Ethical statement This report is based on published and unpublished evidence for predation in the wild. No experimental animals were used for this research.

Acknowledgments Jon Campbell, Phil DeVries, Harry Greene, Bob Henderson, Mahmood Sasa, and Roosevelt García patiently answered numerous questions about decades-old observations and provided supporting notes, voucher material, video clips, and photographs. Darrel Frost allowed me to examine specimens preserved in the AMNH herpetology collection.

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