Australian Field Ornithology 2014, 31, 150–158

Consumption of Pawpaw Carica papaya foliage by Imperial-Pigeons Ducula whartoni: Health or hunger?

John C.Z. Woinarski

National Environmental Research Program Northern Hub, Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin NT 0909, Australia Email: [email protected]

Summary. The ecology of the endemic Imperial-Pigeon occurring on Christmas Island, Ducula whartoni, is poorly known. Here, I report repeated episodes of consumption of leaves of the introduced Pawpaw Carica papaya in observations across the period July 2012 to June 2013. Folivory is unusual in the predominantly frugivorous Ducula fruit-pigeons. There may be three reasons for such regular folivory: (1) leaves were taken when fruit was unavailable or severely limited, (2) fruit was available but provided inadequate nutrition, or (3) fruit was available and adequately nutritious, but Pawpaw leaves were consumed because of their therapeutic value. This study did not provide sufficient critical evidence to test these alternatives.

Introduction The large (c. 600 g) Christmas Island Imperial-Pigeon Ducula whartoni is endemic to the 135-km2 Christmas Island in the Indian Ocean (Higgins & Davies 1996). As with other Ducula species (e.g. Goodwin 1970), it is generally considered an obligate frugivore, although some species in the genus are known ‘to eke out their fruit diet with young foliage’ (Goodwin 1970, p. 384). With the exception of a brief reconnaissance study (Crome 1978), there has been no targeted research on the ecology of the Christmas Island Imperial-Pigeon, and its diet is considered to be ‘poorly known’ in the most substantial account of the species (Higgins & Davies 1996). That consolidated account lists its known diet as comprising fruits of 12 species, but also includes unpublished records of consumption of leaves of three species—Tahitian Chestnut Inocarpos fagifer, White Cedar Melia azedarach and an unspecified plant species in the family Caesalpinaceae. Subsequently, James & McAllan (2014) added two items to the diet reported by Higgins & Davies (1996): young foliage of the introduced Coffee Bush leucocephala and male flowers of Pawpaw Carica papaya. Previous accounts have reported that ‘the food is the fruit and leaf-buds of the various forest ’ (Sharpe 1900, p. 38), that ‘the diet consists almost entirely of small berries’ (Gibson-Hill 1947, p. 98), and that it is ‘known to feed on fruits, buds and young leaves’ (Goodwin 1970, p. 408, but based on previous documentation). Here, I report repeated observations of Christmas Island Imperial-Pigeons consuming mature foliage of the Pawpaw. These observations profer a small contribution to our limited knowledge of this species, but it is possible that they Why do Christmas Island Imperial-Pigeons eat Pawpaw leaves? 151

A

B C

D E

Figure 1. Photographs of Christmas Island Imperial-Pigeons feeding on Pawpaw leaves. Note the jagged leaf in the foreground of (B) caused by repeated tearing for consumption. Photos: John C.Z. Woinarski 152 Australian Field Ornithology J.C.Z. Woinarski also may offer some clue to the current rapid but largely unexplained decline of many endemic Christmas Island species (Smith et al. 2012), including a recent decline in the Island’s only other vertebrate frugivore, the Christmas Island Flying-fox Pteropus melanotus natalis (James et al. 2007; Woinarski et al. 2014). One of the candidate factors in this latter decline may be depletion of food resources (longer or more periods of limited fruit availability) arising from vegetation loss (clearing) or more complex but broad-scale vegetation change due to the impacts of the introduced Yellow Crazy gracilipes (O’Dowd et al. 2003). Another candidate factor may be an undiagnosed disease. There is no compelling direct evidence for either of these factors, and the observations offered here do not claim to provide any definitive case for either, but simply a small piece of the jigsaw. The limited extent to which the observations here may provide inference on causes of decline or loss of other Christmas Island species is constrained further because the status of the Christmas Island Imperial-Pigeons is now apparently stable (James & Retallick 2007; Garnett et al. 2011; James & McAllan 2014), after many decades in which the population was threatened by hunting for human consumption (Chasen 1933; Gibson-Hill 1947; Crome 1978; Stokes 1988), so its ecology may not be a useful analogue for seeking causality behind the decline of other species.

Study area and methods Study area Christmas Island is an isolated oceanic island in the north-eastern Indian Ocean. It was settled in 1888, and subsequent clearing (mostly for mining and residential development) has resulted in loss of ~25% of the Island’s original vegetation cover. The original and remaining vegetation is mostly tall rainforest. Floristic richness is relatively low, with 441 plant species (including 174 naturalised) reported (Du Puy 1993). Of 118 of the most common 213 native species, 35 bear fleshy fruits (Claussen 2005). Christmas Island has an average annual rainfall of ~2100 mm, with rain falling throughout the year but particularly in the months November to June. Over the period considered here, the months of July to November 2012 were unusually dry, and those of April to June 2013 were unusually wet (Table 1).

Pawpaw on Christmas Island Pawpaw (papaya) is a native of , but is now very widely naturalised in tropical areas. It was introduced to Christmas Island within 10 years of initial settlement of the Island (Andrews 1900a; Ridley 1906), and is now widely spread in disturbed areas and rainforest edges. Its leaves are large and palmate.

Methods The foraging of Christmas Island Imperial-Pigeons was observed opportunistically over a period of c. 12 months (July 2012–June 2013) from a verandah overlooking a garden on a hill slope, at Silver City, one of the small suburbs of the Island’s only settlement. Over that period, I looked over the garden for periods of at least 2–3 h on ~40 occasions. The garden Why do Christmas Island Imperial-Pigeons eat Pawpaw leaves? 153 included a range of native and introduced shrub and species, including three Pawpaw shrubs (strictly a ‘large perennial herb’ rather than a shrub: Ayoola & Adeyeye 2010) of heights of 3–4 m. The crowns of these Pawpaw shrubs were at about eye-level and 1–5 m from my observation point on the verandah.

Observations Christmas Island Imperial-Pigeons were observed feeding in the garden on 15 of the ~40 sampling periods. On most occasions, this involved a single bird, but two birds were seen feeding ~2–3 m apart on three occasions, and three birds (also ~2–3 m apart) on one occasion. In all cases, the birds fed only on foliage of Pawpaw, with most observations from only one of the three Pawpaw shrubs. On most occasions, the Pawpaws also had flowers (male or female) and ripe and unripe fruit, but these were not consumed. Generally, the Christmas Island Imperial-Pigeons fed for periods of c. 10–30 minutes, during which they repeatedly used their beaks to rip off pieces (of ~2–5 cm × 2–5 cm) from the outer margins of mature Pawpaw leaves, manipulated these fragments in their beaks and then swallowed the entire leaf portion. Typically, ~5–10 pieces were ripped off and swallowed in succession from a single leaf, and then the bird moved to another leaf in the shrub. Occasionally, ripping resulted in a leaf fragment that was >~5 cm × 5 cm, and this was subsequently dropped. On most occasions, individual birds consumed ~10–20 pieces of leaf before flying off; the highest recorded count was 35 pieces. Sections of leaf were picked off from the leaf periphery, typically leaving the central fibrous midrib (see Figure 1).

Table 1. Rainfall (mm) on Christmas Island over the study period compared with monthly average rainfall (data from Bureau of Meteorology, http://www.bom.gov.au).

Month Recorded in 2012–2013 Long-term average

July 13 96 August 1 42 September 4 44 October 1 65 November 90 147 December 250 216 January 239 301 February 376 347 March 225 299 April 410 224 May 478 182 June 514 163

Total 2601 2126 154 Australian Field Ornithology J.C.Z. Woinarski

There was no marked seasonality in the foraging: I recorded feeding on Pawpaw leaves on three occasions in July–September 2012, four occasions in October– December 2012, three occasions in January–March 2013, and five occasions in April–June 2013, and the number of my observation periods was more or less constant over that period.

Discussion The brief observations reported here add a little to the meagre available information about the ecology of this narrowly endemic bird species, stimulate a question about why foliage of this particular plant species may be so regularly and selectively consumed, and perhaps offer some speculative insight into conservation issues on Christmas Island generally. Pawpaw foliage has not been reported previously in the diet of the Christmas Island Imperial-Pigeon, although there are thinly-documented records of consumption of leaves of four other plant species (Higgins & Davies 1996; James & McAllan 2014). Given that there are documented records of fruit-consumption from only 12 plant species (although this is likely to be a severe under-recording of the diversity of fruits eaten), this suggests that foliage may have importance as a dietary source for this species that is unusual in a Ducula species (Goodwin 1970). There are very few bird species that are obligate arboreal folivores, because the requirement to consume a large volume of energy-poor food would compromise the energetic constraints imposed by flight (Morton 1978). Some facultatively folivorous bats reduce this problem by masticating leaves, ingesting the liquid fraction and expelling as a bolus the fibrous residue, allowing intake of nutrients while minimising the weight cost (Kunz & Ingalls 1994). This was not the case in this study, where Christmas Island Imperial-Pigeons consumed the entire leaf fragment. Why then do Christmas Island Imperial-Pigeons consume Pawpaw leaves? There may be three reasons: (1) fruit may be temporarily unavailable, (2) fruit may be available but insufficiently nutritious, or lacking in some other components, or (3) fruit may be available and provide sufficient nutrition, but the Christmas Island Imperial-Pigeons may be in ill-health or be seeking to prevent ill-health. This very limited study cannot test these hypotheses, but some speculation is possible, and the three potential reasons are now discussed in turn.

Fruit may be temporarily unavailable For primarily frugivorous , the largely constant availability of leaves provides a notable contrast to the typically much more dynamic availability of fruit, and leaves may provide a food resource during periods when fruit is unavailable (Nelson et al. 2000). Christmas Island is a reasonably small island and has relatively few plant species that produce fleshy fruits, so it is feasible that there may be periods during which the sequential availability of fruits from different plant species is interrupted and hence there is little or no fruit available to frugivores. This may be particularly so if phenological patterns are disrupted by Why do Christmas Island Imperial-Pigeons eat Pawpaw leaves? 155 abnormally long periods of rain or of absence of rain. In favour of this explanation is the direct evidence reported within a few years of the onset of human settlement of Christmas Island (and hence before any major environmental modification of the Island), that the Christmas Island Imperial-Pigeon ‘sometimes dies in large numbers for want of sufficient food and water’ (Andrews 1900b, p. 302), although this observation is perhaps unhelpfully ambiguous concerning the cause of mortality. The continuous availability of fruit may be further jeopardised by substantial clearing of native vegetation (Price et al. 1999), and the loss of ~25% of native vegetation (rainforest) on Christmas Island, mostly in the 1960s and 1970s, would have exacerbated any underlying pattern of fruit shortage. To some extent counteracting the impacts of clearing, however, human settlement has also resulted in the introduction and wide spread of many fruiting trees, notably including the Japanese Cherry Muntingia calabura, whose fruit is now a staple food resource for both the Christmas Island Imperial-Pigeon and the Christmas Island Flying- fox (Tidemann 1985; Stokes 1988; James et al. 2007; James & McAllan 2014). A detailed phenological study (Green 1993) at several small sites on Christmas Island found that at least some fruit was available year-round, at least over the 2-year period of that study. Of course, this does not necessarily mean that what fruit was available was suitable for or attractive to Christmas Island Imperial- Pigeons. Furthermore, the relatively even spread throughout the year of my observations of Christmas Island Imperial-Pigeons feeding on Pawpaw foliage suggests that it may be unlikely to be a response to an unusual seasonal nadir in fruit availability, although the atypical rainfall patterns across the study period may have influenced normal phenological patterning, and my sample size is small.

Fruit may be available but provide insufficient nutrients Compared with most fruit, leaves generally provide higher concentrations of minerals and protein (Courts 1998; Nelson et al. 2000) and may be especially rich in calcium (Nelson et al. 2005). Research on some bat and bird species has demonstrated selective consumption amongst plant species of leaves that are relatively rich in nutrient concentrations (Kunz & Diaz 1995; Bucher et al. 2003). Pawpaw leaves may be particularly nutritious: they have been reported to be a rich source of minerals, including calcium, magnesium, sodium, potassium, iron and manganese (Ayoola & Adeyeye 2010). Furthermore, with a leaf protein content of 7% fresh weight, they are amongst the most nutritious 5% of >100 plant species tested by Rao & Polacchi (1972). There is no direct evidence that Christmas Island Imperial-Pigeons are (or are not) nutritionally stressed. If they are, it may be most critical during the breeding season and hence Pawpaw folivory could be expected to increase then. The breeding season is imperfectly known but probably very long; it may peak in about December–April (Gibson-Hill 1947). The lack of clear seasonality in the observations reported here does not support an explanation based on increased 156 Australian Field Ornithology J.C.Z. Woinarski nutritional requirements during the breeding season, but there was little rigour in my seasonal sampling. Furthermore, the Imperial-Pigeon’s reproductive output is relatively low (typically one egg is laid), so the requirement for extra nutritional demands may be limited.

Fruit may be available and nutritious; instead, Pawpaw folivory is used for health reasons In addition to their nutritional value, Pawpaw leaves have high concentrations of alkaloids and ascorbic acid (Ayoola & Adeyeye 2010), and are widely used as an ethnomedicine, including for cancer, infectious diseases and asthma, and as an antibacterial and antifungal agent. There is substantial support for the efficacy of much of this treatment from recent laboratory and other medical trials (Otsuki et al. 2010; Baskaran et al. 2012). However, there is no direct evidence relating to the health status of Christmas Island Imperial-Pigeons, or of the possible health benefits to them from the consumption of Pawpaw foliage. Conversely, Pawpaw leaves also contain saponins that may have cytotoxic effects (Ayoola & Adeyeye 2010), so excessive consumption of the leaves may be detrimental.

Conclusion The information here is inadequate to discriminate between the three possible reasons for repeated folivory by the Christmas Island Imperial-Pigeon. Further research focussed on phenological patterns, landscape-scale fruit availability and nutritional and toxicological status of native and introduced fruits, and of the health and nutritional status of these birds, is desirable because the pattern of folivory observed here may indicate some stress in the ecology of this species. Furthermore, clarification of the causality for folivory here may provide insight into the factors currently contributing to the decline of the Island’s other main vertebrate frugivore, the Christmas Island Flying-fox, and comparable studies on the ecology of that species are desirable. If episodic fruit shortages are the cause of folivory for the Christmas Island Imperial-Pigeon, then any further vegetation clearing may exacerbate the problem. Although appropriate comparative information is not readily available, it may be that, relative to comparable mainland areas, small islands typically have a constrained diversity and abundance of that produce fleshy fruits, and hence may be more likely to have resource bottlenecks for frugivores. In such cases, island frugivores may typically be more generalist in their diets (particularly to more regularly consume items other than fruit) than mainland relatives; and several studies have reported periods of folivory in mainly frugivorous birds on islands, including for the Madeira Laurel Pigeon Columba trocaz (Oliveira et al. 2002) and the Parea (Chatham Island Pigeon) Hemiphaga novaeseelandiae chathamensis (Powlesland et al. 1997). Why do Christmas Island Imperial-Pigeons eat Pawpaw leaves? 157

Acknowledgements I thank David James and Pete Green for relating some of their own observations on the feeding of Christmas Island Imperial-Pigeons, and for comments on a draft of this manuscript. I thank also the editor (James Fitzsimons) and an anonymous referee for additional comments that improved the manuscript.

References Andrews, C.W. (1900a). History and physical features. In: Andrews, C.W. (Ed.). A Monograph of Christmas Island (Indian Ocean), pp. 1–21. British Museum (Natural History), London. Andrews, C.W. (1900b). The geographical relations of the flora and fauna of Christmas Island. In: Andrews, C.W. (Ed.). A Monograph of Christmas Island (Indian Ocean), pp. 299–317. British Museum (Natural History), London. Ayoola, P.B. & Adeyeye, A. (2010). Phytochemical and nutrient evaluation of Carica papaya (pawpaw) leaves. International Journal of Research and Reviews in Applied Sciences 5, 325–328. Baskaran, C., Ratha bai, V., Velu S. & Kumaran, K. (2012). The efficacy of Carica papaya leaf extract on some bacterial and a fungal strain by well diffusion method. Asian Pacific Journal of Tropical Disease 2 (Supplement 2), S658–S662. Bucher, E.H., Tamburini, D., Abril, A. & Torres, P. (2003). Folivory in the white-tipped plantcutter Phytotoma rutila: Seasonal variations in diet composition and quality. Journal of Avian Biology 34, 211–216. Chasen, F.N. (1933). Notes on the fauna of Christmas Island, Indian Ocean. Bulletin of the Raffles Museum 8, 51–87. Claussen, J. (2005). Native Plants of Christmas Island. Supplementary Series no. 22. Australian Biological Resources Study, Canberra. Courts, S.E. (1998). Dietary strategies of Old World fruit bats (Megachiroptera, Pteropodidae): How do they obtain sufficient protein? Mammal Review 28, 185–194. Crome, F.H.J. (1978). Report on the Christmas Island Imperial Pigeon. Unpublished report to Australian National Parks & Wildlife Service, Canberra. Du Puy, D.J. (1993). Christmas Island. In: George, A.S., Orchard, A.E. & Hewson, H.J. (Eds). Flora of Australia Volume 50: Oceanic Islands 2, pp. 1–42. Australian Government Publishing Service, Canberra. Garnett, S.T., Szabo, J.K. & Dutson, G. (2011). The Action Plan for Australian Birds 2010. CSIRO Publishing, Melbourne. Gibson-Hill, C.A. (1947). Notes on the birds of Christmas Island. Bulletin of the Raffles Museum 18, 87–165. Goodwin, D. (1970). Pigeons and Doves of the World. Trustees of the British Museum (Natural History), London. Green, P.T. (1993). The Role of Red Land Crabs (Gecarcoidea natalis (Pocock 1888): Brachyura, Gecarcinidae) in Structuring Rain Forest on Christmas Island, Indian Ocean. PhD thesis. Monash University, Melbourne. Higgins, P.J. & Davies, S.J.J.F. (Eds) (1996). Handbook of Australian, New Zealand & Antarctic Birds, Volume 3: Snipe to Pigeons. Oxford University Press, Melbourne. James, D.J. & McAllan, I.A.W. (2014). The birds of Christmas Island, Indian Ocean: A review. Australian Field Ornithology 31 (supplement), S1–S175. James, D.J. & Retallick, K. (2007). Christmas Island Biodiversity Monitoring Programme: Forest birds of Christmas Island: A Baseline Survey of Abundance. Report to Department of Finance & Administration and Department of Environment & Water Resources. Parks Australia North, Christmas Island. 158 Australian Field Ornithology J.C.Z. Woinarski

James, D.J., Dale, G.J., Retallick, K. & Orchard, K. (2007). Christmas Island flying-fox Pteropus natalis Thomas 1887: An Assessment of Conservation Status and Threats. Report to Department of Finance & Administration and Department of Environment & Water Resources. Parks Australia North, Christmas Island. Kunz, T.H. & Diaz, C.A. (1995). Folivory in fruit-eating bats, with new evidence from Artibeus jamaicensis (Chiroptera: Phyllostomoidae). Biotropica 27, 106–120. Kunz, T.H. & Ingalls, K.A. (1994). Folivory in bats: An adaptation derived from frugivory. Functional Ecology 8, 665–668. Morton, M.S. (1978). Avian folivores: Why not? In: Montgomery, G.C. (Ed.). The Ecology of Arboreal Folivores, pp. 123–130. Smithsonian Institution Press, Washington DC. Nelson, S.L., Kunz, T.H. & Humphrey, S.R. (2005). Folivory in fruit bats: Leaves provide a natural source of calcium. Journal of Chemical Ecology 31, 1683–1691. Nelson, S.L., Miller, M.A., Heske, E.J. & Fahey, G.C. Jr (2000). Nutritional quality of leaves and unripe fruit consumed as famine foods by the flying foxes of Samoa. Pacific Science 54, 301–311. O’Dowd, D.J., Green, P.T. & Lake, P.S. (2003). Invasional ‘meltdown’ on an oceanic island. Ecology Letters 6, 812–817. Oliveira, P., Marrero, P. & Nogales, M. (2002). Diet of the endemic Madeira Laurel Pigeon and fruit resource availability: A study using microhistological analyses. Condor 104, 811–822. Otsuki, N., Dang, N.H., Kumagai, E., Kondo, A., Iwata, S. & Morimoto, C. (2010). Aqueous extract of Carica papaya leaves exhibits anti-tumor activity and immunomodulatory effects. Journal of Ethnopharmacology 127, 760–767. Powlesland, R.G., Dilks, P.J., Flux, I.A., Grant, A.D. & Tisdall, C.J. (1997). Impact of food abundance, diet and food quality on the breeding of the fruit pigeon, Parea Hemiphaga novaeseelandiae chathamensis, on Chatham Island, New Zealand. Ibis 139, 353–365. Price, O.F., Woinarski, J.C.Z. & Robinson, D. (1999). Very large area requirements for frugivorous birds in monsoon rainforests of the , Australia. Biological Conservation 91, 169–180. Rao, M.N. & Polacchi, W. (1972). Food Composition Table for Use in East Asia. US Government Printing Press, Washington DC. Ridley, H.N. (1906). The botany of Christmas Island. Journal of the Straits Branch Royal Asiatic Society 45, 156–271. Sharpe, R.B. (1900). Aves. In: Andrews, C.W. (Ed.). A Monograph of Christmas Island (Indian Ocean), pp. 37–50. British Museum (Natural History), London. Smith, M.J., Cogger, H., Tiernan, B., Maple, D., Boland, C., Napier, F., Detto, T. & Smith, P. (2012). An oceanic island reptile community under threat: The decline of reptiles on Christmas Island, Indian Ocean. Herpetological Conservation and Biology 7, 206–218. Stokes, T. (1988). A Review of the Birds of Christmas Island, Indian Ocean. Occasional paper no. 16. Australian National Parks & Wildlife Service, Canberra. Tidemann, C.R. (1985). A Study of the Status, Habitat Requirements and Management of the Two Species of Bat on Christmas Island (Indian Ocean). Australian National University, Canberra. Woinarski, J.C.Z., Flakus, S., James, D.J., Tiernan, B., Dale, G.J. & Detto, T. (2014). An island-wide monitoring program demonstrates decline in reporting rate for the Christmas Island flying-fox Pteropus melanotus natalis. Acta Chiropterologica 16, 117–127.

Received 13 December 2013