Herpetology Notes, volume 10: 493-496 (2017) (published online on 14 September 2017)

First evidence of nectarivory by four-clawed gecko, Gehyra mutilata (Wiegmann, 1834) (Squamata: Gekkonidae) on a bat- pollinated Calabash tree (Crescentia cujete L.) (Bignoniaceae) in Southcentral Mindanao, Philippines

Krizler Cejuela Tanalgo1,2,* and Alice Catherine Hughes1

In the tropics, vertebrates play an important role introduced across Asia (Burger and Gentry, 2000; as pollinators in many ecosystems. Rodents, birds, Arango-Ulloa et al., 2009). It usually grows in lowland and bats are the best-known vertebrate pollinators in and semi-evergreen tropical forests (Gentry, 1980, 1992) tropical regions (Nabhan and Buchmann, 1997). Apart and is cultivated in many gardens for aesthetic purposes from these, many lizard species have been documented and natural fences and medicines (Heinrich et al., 1998; to feed on flowers and potentially act as a pollinator Reyes and Rosado, 2000; Das et al., 2014). The Long- (Godínez-Álvarez, 2004). Yet, lizard pollination remains Nosed Bat, Glossophaga soricina (Pallas, 1766) has been understudied since the beginning of the 20th century reported as a pollinator of C. cujete in the Neotropics (Olesen and Valido, 2003). At present, there are 34 (Lemke, 1984; Lemke, 1985). In the Paleotropics, the species of lizards known to feed on nectar and flowers pollinators of this species remain understudied, but the of 97 known plant species (Godínez-Álvarez, 2004). Dagger-toothed Nectar Bat Macroglossus minimus (É. Presumably, lizards feeding on nectar are effective Geoffroy, 1810) was observed by the first author to visit pollinators because they transport pollen grains from the flowers of C. cujete. In May 2016, we discovered one flower to another (Godínez-Álvarez, 2004). There that the introduced gecko Gehyra mutilata (Wiegmann, are several examples of lizard species which are known 1834) visits the flowers of C. cujete during the evening, to transport pollen such as Podarcis lilfordi (Günther, and we subsequently documented this behaviour over a 1874) which was observed to carry pollen grains of period of seven months. Euphorbia dendroides L. (Traveset and Saez, 1997) and Photo and video documentation of the gecko-plant Crithmum maritimum L. (Perez-Mellado and Casas, interaction was conducted between mid-2016 to early- 1997). Geckos of the genus Hoplodactylus collect large 2017 in the lowland rural area at Bagumbayan, Tulunan, amounts of pollen on their throats and transport it up to North Cotabato, Philippines (6.8444°N, 124.8788°E). at least 50 m for 12 hours to another flower (Whitaker, We recorded the habit and behavior of G. mutilata to 1987). determine if the observed behaviour was opportunistic The calabash tree (Crescentia cujete L., 1753) is a or a regular interaction between the plant and the gecko perennial species, native to tropical America and widely (see supplementary file for full video documentation). A single flowering C. cujete tree with a height of approximately 6 m was regularly monitored from 1900– 0000 h. Individuals of G. mutilata started their activity at around 2000 h when the flowers of C. cujete were 1 Landscape Ecology Group, Center for Integrative fully open and started to emit a pungent sulphurous Conservation, Xishuangbanna Tropical Botanical Garden, odour. Chinese Academy of Sciences, Menglun, Mengla, 666909 The feeding activity of the geckos started by locating Yunnan, People’s Republic of China a fully-opened, cauliflorous flower (Fig. 1A,B). 2 Department of Biological Sciences, College of Arts and Sciences, University of Southern Mindanao, Kabacan, 9407 After an individual gecko had located a target flower, North Cotabato, The Philippines it moved to the outer part of the flower (Fig. 1C–E), * Corresponding Author. E-mail: [email protected] presumably to check the presence of available nectar. 494 Krizler Cejuela Tanalgo & Alice Catherine Hughes

Figure 1. Nectarivory of Gehyra mutilata on flowers of Crescentia cujete in south-central Mindanao, the Philippines. (A,B) Images demonstrating the ‘locating’ behaviour stage of the Gehyra mutilata-plant interaction. During this stage, one or two G. mutilata locate and move towards C. cujete flowers, selecting the potential flower to feed on, and observing potential competitors. (C–E) An individual G. mutilata is shown as it tests a flower of C. cujete. (F–H) Images showing the last stage of nectarivory, the ‘foraging’ activity. An individual of G. mutilata enters the flower to at least one third of its body length to reach the nectar. (I) Gehyra mutilata carrying pollen grains on its throat after consuming the nectar of C. cujete. Photos by K.C. Tanalgo.

In some observations, individual G. mutilata moved on easily reached cauliflorous flowers laying on stems or to another flower without feeding on the first one. After hanging down from different heights. The feeding on the individual gecko found a target flower, it moved an individual flower usually lasted a few minutes, after at least a third of its body inside it and started feeding which a gecko moved along the branches to look for (Fig. 1G,H). Gehyra mutilata are good climbers and another flower. Flowers were not visited by more than First evidence of nectarivory by Gehyra mutilata in the Philippines 495 one individual G. mutilata at the same time. Geckos his insightful comments on the early findings of this study. We remained active until 0100 h when flowers started to are also grateful to C. Tanalgo and I. Tanalgo for the assistance close their petals. during the field observations. This is the first documented evidence of G. mutilata feeding on C. cujete, a species that is otherwise known References to be pollinated by bats. Gehyra mutilata is widely Arango-Ulloa, J., Bohorquez, A., Duque, M.C., Maass, B.L. distributed throughout Southeast Asia and other tropical (2009): Diversity of the calabash tree (Crescentia cujete L.) in regions (e.g., Fisher, 1997; Devan-Song and Brown, Colombia. Agroforestry Systems 76: 543–553. 2012). It is a nocturnal predator of small insects and Barragán-Ramírez, J.L., Reyes-Luis, O.E., de Jesús Ascencio- common in urbanized areas (Devan-Song and Brown, Arrayga, J., Navarrete-Heredia, J.L., Vásquez-Bolaños, M. 2012). A recent comprehensive diet analysis revealed that (2015): Diet and reproductive aspects of the exotic gecko Gehyra mutilata (Wiegmann, 1834) (Sauria: Gekkonidae) in G. mutilata mainly consumes arthropods, particularly the urban area of Chapala, Jalisco, Mexico. Acta Zoológica Diptera (Nematocera), and has never been recorded Mexicana, Nueva Serie 31: 67–73. to feed on nectar (Barragán-Ramírez et al., 2015). In Bègue, J.F., Sanchez, M., Micheneau, C., Fournel, J. (2014): New the family Gekkonidae, the genera Hoplodactylus, record of day geckos feeding on orchid nectar in Reunion Island: Naultinus, and Phelsuma have been recorded and can lizards pollinate orchid species? Herpetology Notes 7: 689– are known as nectar feeders and potential pollinators 692. (Whitaker, 1987; Nyhagen et al., 2001). The day gecko Burger, W., Gentry, A.H. (2000): Crescentia Linnaeus. Flora Costaricensis, Fieldiana Botany New Series 41: 118–121 Phelsuma mutabilis (Grandidier, 1869) was observed Das, N., Islam, M.E., Jahan, N., Islam, M.S., Khan, A., Islam, M.R., to feed on the nectar of the mangrove tree Sonneratia Parvin, M.S. (2014): Antioxidant activities of ethanol extracts alba Smith, 1816 from southwest Madagascar (Taylor and fractions of Crescentia cujete leaves and stem bark and the and Gardner, 2014), and Phelsuma borbonica Mertens, involvement of phenolic compounds. BMC Complementary 1966 was reported to feed on the nectar of the orchid and Alternative Medicine 14: 1–9. Angraecum cadetii Bosser, 1988 (Bègue et al., 2014). Devan-Song, A., Brown, R.M. (2012): Amphibians and reptiles of Luzon Island, Philippines. VI. The herpetofauna of the Subic On this occasion, we did not examine the pollination Bay Area. Asian Herpetological Research 3: 1–20. role of G. mutilata but observed that pollen sticking to the Fisher, R.N. (1997): Dispersal and evolution of the Pacific gecko’s snout and body came in contact with the flowers’ Basin gekkonid lizards Gehyra oceanica and Gehyra stigmata (Fig. 1F,G) which indicates that G. mutilata mutilata. Evolution 51: 906–921. is a potential pollinator of C. cujete. Additionally, we Gentry, A.H. (1980): Crescentia. Bignoniaceae, Part I (Crescentieae observed few G. mutilata individuals carrying pollen and Tourretieae), Flora Neotropical Monograph 25: 82–96. Godínez-Álvarez, H. (2004): Pollination and seed dispersal by grains of C. cujete on their throats (Fig. 1I), similar to lizards: a review. Revista Chilena de Historia Natural 77: 569– other nectarivorous gecko. The capacity of the gecko to 577. transfer pollen from the anther to the stigma remains to Heinrich, M., Ankli, A., Frei, B., Weimann, C., Sticher, O. (1998): be studied in further investigations. Nonetheless, similar Medicinal plants in Mexico: Healers’ Consensus and Cultural observations of the gekkonid species Hoplodactylus Importance. Social Science & Medicine 47: 1859–1871. duvauceli (Duméril and Bibron, 1836), Woodworthia Lemke, T.O. (1984): Foraging ecology of the long-nosed maculata (Gray, 1845), and Phelsuma ornata Gray, bat, Glossophaga soricina, with respect to resource availability. Ecology 65: 538–548. 1825 found that these species deposit on their throats a Lemke, T.O. (1985): Pollen carrying by the nectar-feeding bat considerable amount of pollen grains of the flowers they Glossophaga soricina in a suburban environment. Biotropica visit (Sáez and Traveset, 1995; Godinez-Alvarez, 2004). 17: 107–111. We hope that our observation will encourage ecologists Nabhan, G.P., Buchmann, S.L. (1997): Services provided by to further explore this previously undocumented plant- pollinators. In: Nature’s Services: Societal Dependence on animal interaction. The only known pollinator of C. Natural Ecosystems, p. 133–150. Daily, G.G, Ed., Washington, D.C., USA, Island Press. cujete is a nectarivorous bat from the Neotropics and it Nyhagen, D.F., Kragelund, C., Olesen, J.M., Jones, C.G. (2001): will be interesting to investigate how the Calabash Tree Insular interactions between lizards and flowers: flower is pollinated in the absence of its natural pollinators. visitation by an endemic Mauritian gecko. Journal of Tropical Ecology 17: 755–761. Acknowledgement. The authors are grateful to Richard T. Olesen, J.M., Valido, A. (2003): Lizards as pollinators and seed Corlett, (Center for Integrative Conservation, Xishuangbanna dispersers: an island phenomenon. Trends in Ecology and Tropical Botanical Garden, Chinese Academy of Sciences) for Evolution 18: 177–181. 496 Krizler Cejuela Tanalgo & Alice Catherine Hughes

Pérez-Mellado, V., Casas, J.L. (1997): Pollination by a lizard on a Mediterranean island. Copeia 1997: 593–595. Reyes, S.A., Rosado, I.C. (2000): Plantas utilizadas como cercas vivas en el estado de Veracruz. Madera y Bosques 6: 55–71. Taylor, B., Gardner, C. (2014): Nectar feeding by the day gecko Phelsuma mutabilis (Squamata: Gekkonidae) on the mangrove tree Sonneratia alba (Lythraceae) in southwest Madagascar. Herpetology Notes 7: 85–87. Traveset, A., Sáez, E. (1997): Pollination of Euphorbia dendroides by lizards and insects: spatio-temporal variation in patterns of flower visitation. Oecologia 111: 241–248. Whitaker, A. H. (1987): The roles of lizards in New Zealand plant reproductive strategies. New Zealand Journal of Botany 25: 315–328.

Supplementary Video A supplementary video documentation of the nectarivory of Gehyra mutilata on C. cujete tree was deposited and accessible from here: https://doi. org/10.6084/m9.figshare.5285995.v1.

Accepted by Maximilian Dehling