Abstract
Japanese giant flying squirrels, Petaurista leucogenys, are entirely arboreal folivores. From spring to summer, their principal food source consists of leaves of the deciduous oak Quercus acutissima in western Tokyo, Japan. Before consuming the central part of each leaf, the squirrels fold the leaf two or more times with their forelegs. In the wild, leaf folding is a very rare behavior, even in primates. In our study, this peculiar feeding behavior was not observed across all study sites or even in some local populations. Herbivores generally try to maximize their intake of nutritious foods (e.g., sugars) containing low levels of plant defensive chemicals (e.g., phenols). We found that total phenolic contents in individual leaves of Q. acutissima were lower in the center than at the margins, whereas sugar (glucose) was homogenously distributed. Consequently, consumption of only leaf centers appears to be an adaptation by Japanese giant flying squirrels to avoid leaf margin defensive chemicals and structures. These leaf margin characteristics, which may have developed as defenses against herbivorous insects that generally feed from the margins, have contributed to the skillful and complex feeding behavior of this generalist folivore.
Similar content being viewed by others
References
Ainser R, Terkel J (1992) Ontogeny of pine cone opening behaviour in black rats, Rattus rattus. Anim Behav 44:327–336
Ando M, Shiraishi S, Uchida T (1985) Food habits of the Japanese giant flying squirrel, Petaurista leucogenys. J Fac Agric Kyushu Univ 29:189–202
Aoki Y, Kasahi T, Shigeta M, Yanagawa M, Hasuda H, Yamaguchi N, Takeuchi T, Kobayashi T, Satoh K, Ninomiya T, Hayakawa H (2006) Distribution of the Japanese giant flying squirrel in Kanagawa Prefecture, Japan. Nat Hist Rep Kanagawa 27:27–40 (in Japanese)
Baba M, Doi T, Ono Y (1982) Home range utilization and nocturnal activity of the giant flying squirrel, Petaurista leucogenys. Jpn J Ecol 32:189–198
Baber O, Slot M, Celis G, Kitajima K (2014) Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species. Botany 92:535–540
Barbehenn RV, Constabel CP (2011) Tannins in plant–herbivore interactions. Phytochemistry 72:1551–1565
Bernays EA (1998) Evolution of feeding behavior in insect herbivores. Bioscience 48:35–44
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509
Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR (2003) Variation in the nutritional value of primate foods: among trees, time periods, and areas. Int J Primatol 24:317–333
Close DC, McArthur C (2002) Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99:166–172
Cooney LJ, van Klink JW, Hughes NM, Perry NB, Schaefer HM, Menzies IJ, Gould KS (2012) Red leaf margins indicate increased polygodial content and function as visual signals to reduce herbivory in Pseudowintera colorata. New Phytol 194:488–497
Covelo F, Gallardo A (2001) Temporal variation in total leaf phenolics concentration of Quercus robur in forested and harvested stands in northwestern Spain. Can J Botany 79:1262–1269
Farmer EE (2014) Leaf defence. Oxford University Press, Oxford
Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581
Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interaction between plants and insects. Springer, New York, pp 1–40
Forkner RE, Marquis RJ, Lill JT (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–187
Garber PA (1987) Foraging strategies among living primates. Ann Rev Anthropol 16:339–364
Glander KE (1982) The impact of plant secondary compounds on primate feeding behavior. Am J Physic Anthropol 25:1–18
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol, Evol Syst 8:157–178
Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501
Hughes NM, Lev-Yadun S (2015) Red/purple leaf margin coloration: potential ecological and physiological functions. Env Exp Bot 119:27–39
Hughes NM, Smith WK, Gould KS (2010) Red (anthocyanic) leaf margins do not correspond to increased phenolic content in New Zealand Veronica spp. Ann Bot 105:647–654
Jensen LM, Wallis IR, Foley WJ (2015) The relative concentrations of nutrients and toxins dictate feeding by a vertebrate browser, the greater glider Petauroides volans. PLoS One 10:e0121584
Karageorgou P, Manetas Y (2006) The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light. Tree Physiol 26:613–621
Kawamichi T (1984a) Sociality of nocturnal Japanese giant flying squirrels, part 1. Shizen 1984:18–26 (in Japanese)
Kawamichi T (1984b) Sociality of nocturnal Japanese giant flying squirrels, part 2. Shizen 1984:64–72 (in Japanese)
Kawamichi T (1997) Seasonal changes in the diet of Japanese giant flying squirrels in relation to reproduction. J Mammal 78:204–212
Kawamichi T (2010) Review: food habits of Petaurista leucogenys. Sciurid Inf 25:11–19 (in Japanese)
Kawamichi T (2015) The Japanese giant squirrel. Tsukiji Shokan Publishing Co. Ltd., Tokyo (in Japanese)
Kohl KD, Miller AW, Dearing MD (2015) Evolutionary irony: evidence that ‘defensive’ plant spines act as a proximate cue to attract a mammalian herbivore. Oikos 124:835–841
Koops K, McGrew WC, Matsuzawa T (2013) Ecology of culture: do environmental factors influence foraging tool use in wild chimpanzees, Pan troglodytes verus? Anim Behav 85:175–185
Laland KN (2008) Animal cultures. Curr Biol 18:R366–R370
Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547
Laska M (1996) Taste preference thresholds for food-associated sugars in the squirrel monkey (Saimiri sciureus). Primates 37:91–95
Lemon CH (2015) Perceptual and neural responses to sweet taste in humans and rodents. Chemosens Percept 8:46–52
Li Y, Ding P, Huang C, Lu S (2015) Total tannin content of foods of François’ langur in Fusui, Guangxi, China: preliminary study. Acta Ecol Sinica 35:16–22
Lu HP, Wang YB, Huang SW, Lin CY, Wu M, Hsieh CH, Yu HT (2012) Metagenomic analysis reveals a functional signature for biomass degradation by cecal microbiota in the leaf-eating flying squirrel (Petaurista alborufus lena). BMC Genom 13:466
Matsuda I, Tuuga A, Bernard H, Sugau J, Hanya G (2013) Leaf selection by two Bornean colobine monkeys in relation to plant chemistry and abundance. Sci Rep 3:1873
Mauffette Y, Oechel WC (1989) Seasonal variation in leaf chemistry of the coast live oak Quercus agrifolia and implications for the California oak moth Phryganidia californica. Oecologia 79:439–445
McFarland D (1981) The Oxford companion to animal behaviour. Oxford University Press, Oxford
Meyer GA (1993) A comparison of the impacts of leaf-and sap-feeding insects on growth and allocation of goldenrod. Ecology 74:1101–1116
Mikuriya M (1993) Fauna in the Tama Forest Science Garden. Bull For For Prod Res Inst 364:97–113 (in Japanese)
Norscia I, Ramanamanjato JB, Ganzhorn JU (2012) Feeding patterns and dietary profile of nocturnal southern woolly lemurs (Avahi meridionalis) in southeast Madagascar. Int J Primatol 33:150–167
Nurmi K, Ossipov V, Haukioja E, Pihlaja K (1996) Variation of total phenolic content and individual low-molecular-weight phenolics in foliage of mountain birch trees (Betula pubescens ssp. tortuosa). J Chem Ecol 22:2023–2040
Ohdachi SD, Ishibashi Y, Iwasa M, Fukui D, Saitoh T (2015) The wild mammals of Japan, 2nd edn. Shoukadoh, Kyoto
Okazaki H (2004) Research for habitat selection in giant flying squirrels along the Tama River. Tokyu Found Better Environ, Grant Award Gen Res 143:1–34 (in Japanese)
Passarinho JA, Lamosa P, Baeta JP, Santos H, Ricardo CP (2006) Annual changes in the concentration of minerals and organic compounds of Quercus suber leaves. Physiol Plant 127:100–110
Potter DA, Kimmerer TW (1988) Do holly leaf spines really deter herbivory? Oecologia 75:216–221
Provenza FD, Villalba JJ, Dziba LE, Atwood SB, Banner RE (2003) Linking herbivore experience, varied diets, and plant biochemical diversity. Small Rumin Res 49:257–274
Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K (2002) Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380–390
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Func Ecol 25:325–338
Shigeta M, Okazaki H (2001) Various leaf debris by Japanese giant flying squirrels. Sciurid Inf 9:10–11 (in Japanese)
Shigeta M, Shoji T, Kasahi T, Ando M (2009) Habitat conditions of an isolated population of the Japanese giant flying squirrel Petaurista leucogenys at Machida, Tokyo. J Jpn Wildl Res Soc 34:37–43 (in Japanese)
Shigeta M, Shigeta Y, Tamura N (2010) Habitat use of giant flying squirrels, Petaurista leucogenys, by collecting their field tracks. J Jpn Wildl Res Soc 35:13–21 (in Japanese)
Soné K, Takano H, Tamura N (1996) Seasonal patterns of the feeding items of the giant flying squirrel, Petaurista leucogenys, and changes in its feeding sites due to the introduction of street lightings in Tama Forest Science Garden. J Jpn For Soc 78:369–375 (in Japanese)
Sousa C, Biro D, Matsuzawa T (2009) Leaf-tool use for drinking water by wild chimpanzees (Pan troglodytes): acquisition patterns and handedness. Anim Cog 12:115–125
Takechi R, Hayashi F (2011) Transmission of walnut-feeding skills from mother to young in wood mice (Apodemus speciosus). Adv Biosci Biotechnol 2:8898
Takechi R, Tamura N, Hayashi F (2009) Improved walnut-feeding skills with experience in wood mice, Apodemus speciosus. J Ethol 27:83–89
Tamura N (2004) Effects of habitat mosaic on home range size of the Japanese squirrel, Sciurus lis. Mamm Study 29:9–14
Tamura N (2011) Population differences and learning effects in walnut feeding technique by the Japanese squirrel. J Ethol 29:351–363
Tonooka R (2001) Leaf-folding behavior for drinking water by wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea. Anim Cog 4:325–334
Weigl PD, Hanson EV (1980) Observational learning and the feeding behavior of the red squirrel Tamiasciurus hudsonicus: the ontogeny of optimization. Ecology 6:213–218
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, New Jersey
Zohar O, Terkel J (1996) Social and environmental factors modulate the learning of pine-cone stripping techniques by black rats, Rattus rattus. Anim Behav 51:611–618
Zucker WV (1982) How aphids choose leaves: the roles of phenolics in host selection by a galling aphid. Ecology 63:972–981
Acknowledgments
We thank John L. Koprowski for providing funding from the University of Arizona BRAVO! undergraduate research program to NS and BR for research in Tokyo during the summer in 2013. We also thank Renee M. Borges for useful information on the leaf feeding patterns of Ratufa squirrels introduced to Kawamichi (2015) and Tamotsu Kusano for helping with the statistical analysis. This study was partly supported by competitive research funding from the Graduate School of Science and Engineering, Tokyo Metropolitan University, to FH in 2015 and by a Sasakawa Scientific Research Grant from the Japan Science Society to MI.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Ito, M., Seto, N., Rico, B. et al. Folivory with leaf folding by giant flying squirrels: its patterns and possible function. Ecol Res 31, 617–626 (2016). https://doi.org/10.1007/s11284-016-1371-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-016-1371-x