Descending from the trees onto the mud to feed: observation of ophiophagy by Trimeresurus purpureomaculatus (Gray, 1832) on - Biotaxa

Herpetology Notes, volume 14: 1281-1285 (2021) (published online on 8 October 2021)

     Descending from the trees onto the mud to feed: observation of
    ophiophagy by Trimeresurus purpureomaculatus (Gray, 1832) on
                  Fordonia leucobalia (Schlegel, 1837)

                                          Alex Figueroa1,* and Ryan J.R. McCleary2

  Ophiophagy, the feeding mode whereby animals prey                bend the vertebral column of the prey snake into
on snakes, is considered exceptional in snakes (Greene,            waves to accommodate it inside the gastrointestinal
1997) aside from a few taxa famed for this dietary                 tract (Jackson et al., 2004).
specialisation, most notably members of the genera                   Vipers, in particular, are not known to engage in
Clelia, Lampropeltis, and Micrurus, as well as the King            ophiophagy as readily as other snakes, as they have
Cobra, Ophiophagus hannah (Cantor, 1836). Colston                  been documented to feed mainly on amphibians, lizards,
et al. (2010) estimated that approximately 20.4%                   birds, and mammals (Cundall & Greene, 2000). The
(~700 species) of all alethinophidian snakes (Uetz et              diet of vipers is mostly attributed to them being more
al., 2021) exhibit ophiophagous behaviour. Numerous                robust and having a large gape capacity relative to other
observations of ophiophagy have been recorded in                   snakes and utilising a sit-and-wait foraging mode. Thus,
other species, but these are generally limited to single           vipers are regarded as feeding less frequently than other
events (e.g., McKelvy et al., 2013; Coelho-Lima et                 snakes. Trimeresurus purpureomaculatus (Gray, 1832) is
al., 2020), undoubtedly due to the secretive nature of             an arboreal pitviper that inhabits mangroves and coastal
snakes that makes witnessing snakes feeding in the wild            environments of southern Myanmar, Thailand, western
challenging. Indeed, much of what is known regarding               Peninsular Malaysia, Singapore, and Sumatra (David
snake diets comes from the examination of museum                   and Vogel, 1996). Aside from being arboreal and feeding
specimens (Glaudas et al., 2017).                                  on frogs, lizards, birds, and small mammals (David
  Theoretically, as gape-limited predators, feeding                and Vogel 1996), Pauwels et al. (2000) reported that a
on elongated prey should be functionally more                      captured individual in Thailand contained the digestive
manageable for snakes than feeding on bulkier prey                 remains of a congener. Otherwise, little is published
with limbs. One hypothesis why ophiophagy is not                   regarding the ecology of T. purpureomaculatus. Herein,
more prevalent in snakes is related to handling time,              we present the first field observation of ophiophagy in
where ingesting elongated prey takes substantially                 T. purpureomaculatus (Fig. 1), in which we observed a
longer than non-elongated prey (Jackson et al., 2004;              juvenile trail, capture, and feed on a Fordonia leucobalia
Banci et al., 2017). Handling time is a function of                (Schlegel, 1837), a mangrove homalopsid (mudsnake)
prey size, and snakes as prey tend to approximate                  that spends a considerable amount of time in mud lobster
or exceed the size of the predatory snake, especially              mounds (Karns et al., 2002). We also discuss a potentially
the consumer’s gut size (Jackson et al., 2004). One                novel form of ophiophagous consumption whereby the
solution to overcoming this challenge is to forcibly               prey is ingested not head or tail first (Jackson et al., 2004;
                                                                   Braz and Marques, 2016), but from the midbody.
                                                                     On the night of 25 November 2014, while surveying
                                                                   Pasir Ris Park Mangroves (PRPM) in Singapore
1
  Department of Biological Sciences, University of New Orleans,
   New Orleans, Louisiana 70122, USA.
                                                                   (1.37789°N, 103.9525°E), we spotted a snake writhing
2
  Protein Science Laboratory, Department of Biological Sciences,   in the mud at around 23:35 h. The snake was a ~30 cm
   Faculty of Science, National University of Singapore, 117543,   snout–vent length (SVL) F. leucobalia that appeared to
   Singapore; and Department of Integrative Biology, University    be in the stages of dying (Fig. 1A). After watching the
   of South Florida, Sarasota, Florida 34243, USA.                 snake for a few seconds, we noticed another snake trailing
*
  Corresponding author. E-mail: afigueroa21@gmail.com              behind it. The second snake we quickly identified as T.
© 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0.       purpureomaculatus (Fig. 1A). It is likely that just prior to

1282                                                                                Alex Figueroa & Ryan J.R. McCleary

our arrival, the ~45 cm SVL viper had envenomated the            incrementally (Fig. 2A). For further support, the viper
mudsnake and was pursuing it. When we first approached,          used its tail to anchor itself against the tree root, switching
the viper seemed to become agitated, retreated a few             from having its tail on its left side to positioning it on its
meters, but quickly resumed its pursuit. By 23:40 h, the         right side for better leverage (Fig. 2B). By 00:25 h, the
viper had reached the mudsnake and began probing along           viper had reached a point in the bend of the mudsnake’s
its body, seemingly trying to find the head (Fig. 1B). This      body where the head and tail began to meet, and the
occurred at the base of a mound, and as the viper seized         head entered the mouth before the tail (Fig. 2C). At
the mudsnake’s head, the rest of the viper’s body elevated       00:27 h, the viper had reached the mudsnake’s tail and
to the top of the mound. At this point, the viper released       finished consuming its meal by 00:29 h (Fig. 2D). Shortly
the mudsnake’s head, grasped it near the middle of its           thereafter, the viper gave a characteristic snake yawn to
body, and hoisted the mudsnake up onto the mound (Fig.           realign its jaws and slowly slithered off. A video showing
1C). In what we believe to be an attempt by the viper to         a portion of the predation event is available at https://
secure a better hold of its prey, the viper slid down a tree     youtu.be/S2OT2fJf6OI.
root that was sticking out of the mud next to it (Fig. 1C).        Our encounter is the first live field observation of
By the end of this action, 15 min had elapsed (time 00:05        ophiophagy in T. purpureomaculatus and the first
h) and the viper commenced ingesting the mudsnake from           observation of a F. leucobalia being eaten by a viperid
the middle of its body (Fig. 1D).                                (Voris and Murphy, 2002). Previously, Pauwels et al.
  The entire ingestion phase lasted 24 min. The viper            (2000) reported that a captured T. purpureomaculatus
began eating the mudsnake in typical viper fashion by            in Thailand contained the digestive remains of
using its fangs to walk along the mudsnake’s body and            another viper, which they identified as a congener. As
using its throat muscles to forcefully ingest the snake          part of a larger study characterizing the venom of T.

Figure 1. A predatory encounter between a mudsnake (Fordonia leucobalia) and mangrove viper (Trimeresurus purpureomaculatus)
in Pasir Ris Park Mangroves, Singapore. (A) The writhing mudsnake (red circle) is being pursued by the viper (blue circle). (B)
The viper seized the mudsnake by its head, but then (C) switched its grasp to midbody in order to hoist its prey up onto a mud
mound to (D) begin eating it. Photographs by Ryan McCleary.

Ophiophagy by Trimeresurus purpureomaculatus on Fordonia leucobalia                                                  1283

Figure 2. A predatory encounter between a mudsnake (Fordonia leucobalia) and mangrove viper (Trimeresurus
purpureomaculatus) in Pasir Ris Park Mangroves, Singapore. (A) The viper is using its fangs to ingest the folded body of the
mudsnake, while (B) positioning its tail on a mangrove root for support. The viper proceeded to consume the mudsnake at
midbody with (C) the head entering the mouth first, before (D) the tail. Photographs by Alex Figueroa.

purpureomaculatus, RJRM gathered an amalgamation                (Karns et al., 2002). Cerberus schneiderii is often the
of snake bones (Fig. 3A), that included vertebrae, ribs,        most abundant snake at any mangrove in Southeast
and scales (Fig. 3B–D) found in faecal samples excreted         Asia (Murphy, 2007), including Sungei Buloh Wetland
from three different T. purpureomaculatus collected at          Reserve in Singapore (Chim and Diong, 2013), Peninsular
PRPM. Mixed in one of the faecal samples was also the           Malaysia (Jayne et al., 1987), and Bangladesh (Rahman
partially digested claw of a crab, indicating the viper had     et al., 2014), constituting a bountiful food source. Thus, if
eaten one of two crustacean-eating homalopsid species, F.       T. purpureomaculatus does indeed prefer to eat snakes, it
leucobalia or Gerarda prevostiana (Eydoux & Gervais,            has at least one dominant species to rely upon.
1837). Our observations, along with that of Pauwels et            The method in which the T. purpureomaculatus ingested
al. (2000), support that T. purpureomaculatus, at least         the F. leucobalia is unusual. Snakes typically consume
occasionally, forages on the ground (David and Vogel,           their prey head-first, but sometimes may ingest prey from
1996), offering the possibility that T. purpureomaculatus       the caudal region (Cundall and Greene, 2000) or tail first
may prey on snakes regularly. Thus, the overarching             in the case of ophiophagy in Erythrolamprus Boie, 1826
question that should be investigated in future studies          (Braz and Marques, 2016). Ingesting the mudsnake from
is whether T. purpureomaculatus prefers feeding on              midbody was likely a failure or carelessness on the part
snakes or whether they are only opportunistically               of the viper to locate the mudsnake’s head, or urgency
consuming snakes, possibly due to restricted availability       to consume its prey. The viper did appear to search for
of preferred prey.                                              the mudsnake’s head but then abandoned the pursuit at
  In Southeast Asia, snakes are a prominent inhabitant          midbody and began ingesting the snake. However, it is
of mangroves. Pasir Ris Park Mangroves is home to at            interesting to propose that perhaps feeding on elongate
least eight other snake species, with Cerberus schneiderii      prey at midbody, with the body of the prey doubled over,
(Schlegel, 1837) being indisputably the most common             may serve as a means of overcoming the biomechanical

1284                                                                                 Alex Figueroa & Ryan J.R. McCleary

Figure 3. Photographs of snake remains found in the faeces of Trimeresurus purpureomaculatus from Pasir Ris Park Mangroves,
Singapore. The remains included (A) a mixture of cranial bones, (B) vertebrae, (C) ribs, and (D) scales. Photographs by Ryan
McCleary.

challenge of accommodating such a long prey item in the         References
gastrointestinal tract (Jackson et al., 2004). Alternatively,   Banci, K.R.S., Viera, N.F.T., Freitas, A.C., Marques, O.A.V. (2017):
ingesting elongated prey from midbody may also serve              Feeding on elongate prey: additional data for the coral snake
to reduce handling time as it took the viper 24 min to            Micrurus corallinus (Merrem, 1820) (Elapidae) and comments
fully ingest the mudsnake. This time is at the lower              on aposematism. Herpetology Notes 10: 335–338.
limit of ingestion time of elongate prey in snakes but          Braz, H.B., Marques, O.A. (2016): Tail-first ingestion of prey by
is still much greater than ingesting non-elongate prey            the false coral snake, Erythrolamprus aesculapii: Does it know
                                                                  where the tail is? Salamandra 52(2): 211–214.
(Banci et al., 2017). Our observation documents the
                                                                Chim, C.K., Diong, C.H. (2013): A mark-recapture study of a
first instance of a viper feeding on a homalopsid, and            dog-faced water snake Cerberus schneiderii (Colubridae:
this substantiates that T. purpureomaculatus descends             Homalopsidae) population in Sungei Buloh Wetland Reserve,
from the trees to forage on the ground. The frequency             Singapore. Raffles Bulletin of Zoology 61: 811–825.
of these behaviours remains unknown and awaits further          Coelho Lima, A.D., Oliveira Ramos, G., Martins, R.B.X., Castro
study. Perhaps, T. purpureomaculatus only uses arboreal           Meira, L.P.D. (2020): Fist record of ophiophagy in the false
settings for escaping the daily mangrove tidal events,            coral snake Oxyrhopus trigeminus Duméril, Bibron & Duméril,
                                                                  1854. Cuadernos de Herpetología, 34(1) 89–91.
evading predators, and basking.
                                                                Cundall, D., Greene, H.W. (2000): Feeding in snakes. In: Feeding:
                                                                  Form, Function, and Evolution in Tetrapod Vertebrates, p. 293–
Acknowledgements. This observation was made during a survey       333. Schwenk, K., Ed., New York, USA, Academic Press.
covered by research permit NP/RP10-095-3b issued to RJRM by     David, P., Vogel, G. (1996): The Snakes of Sumatra, an Annotated
the National Parks Board. We would like to thank John Ascher      Checklist and Key with Natural History Notes. Frankfurt am
at the National University of Singapore for allowing use of       Main, Germany, Edition Chimaira.
his microscope. We also want to thank the reviewers for their   Glaudas, X., Kearney, T.C., Alexander, G.J. (2017): Museum
comments and suggestions, and Jason Fantuzzi for his insight      specimens bias measures of snake diet: a case study using the
into snake feeding.                                               ambush-foraging puff adder (Bitis arietans). Herpetologica
                                                                  73(2): 121–128.

Ophiophagy by Trimeresurus purpureomaculatus on Fordonia leucobalia                                                               1285
Greene, H.W. (1997): Snakes: the Evolution of Mystery in Nature.     Murphy, J.C. (2007): Homalopsid Snakes. Evolution in the Mud.
   Berkeley, California, USA, University of California Press.          Malabar, Florida, USA, Krieger Publishing Company.
Jackson, K., Kley, N.J., Brainerd, E.L. (2004): How snakes           Pauwels, O.S.G., Laohawat, O.-A., David, P., Bour, R., Dangsee,
   eat snakes: the biomechanical challenges of ophiophagy for          P., Puangjit, C., Chimsunchart, C. (2000): Herpetological
   the California kingsnake, Lampropeltis getula californiae           investigations in Phang-Nga Province, southern peninsular
   (Serpentes: Colubridae). Zoology 107(3): 191–200.                   Thailand, with a list of reptile species and notes on their biology.
Jayne, B.C., Voris, H.K., Kiew, B.H. (1987): Diet, feeding             Dumerilia 4: 123–154.
   behavior, growth, and numbers of a population of Cerberus         Rahman, S.C., Reza, A.A., Datta, R., Jenkins, C.L., Luiselli,
   rynchops (Serpentes: Homalopsinae) in Malaysia. Fieldiana           L. (2014): Niche partitioning and population structure of
   Zoology 50: 1–15.                                                   sympatric mud snakes (Homalopsidae) from Bangladesh. The
Karns, D.R., Voris, H.K., Goodwin, T.G. (2002): Ecology of             Herpetological Journal 24(2): 123–128.
   oriental-Australian rear-fanged water snakes (Colubridae:         Uetz, P., Freed, P., Hošek, J. (2019): The Reptile Database.
   Homalopsinae) in the Pasir Ris Park mangrove forest, Singapore.     Available at: http://www.reptile-database.org. Accessed on 21
   Raffles Bulletin of Zoology 50: 487–498.                            March 2021.
McKelvy, A.D., Figueroa, A., Lewis, T.R. (2013): First record        Voris, H.K., Murphy, J.C. (2002): The prey and predators of
   of ophiophagy in the widely distributed snake Leptodeira            homalopsine snakes. Journal of Natural History 36: 1621–1632.
   septentrionalis (Kennicott, 1859) (Ophidia, Colubridae).
   Herpetological Notes 6: 177–178.

                                                                                             Accepted by Justin Bernstein