Mini-Review
Mini-Review
Plant Signaling & Behavior 5:10, 1187-1189; October 2010; © 2010 Landes Bioscience
Mutualism between tree shrews and pitcher plants
Perspectives and avenues for future research Charles Clarke,1,* Jonathan A. Moran2 and Lijin Chin1 School of Science; Monash University Sunway Campus; Bandar Sunway; Selangor, Malaysia; 2School of Environment and Sustainability; Royal Roads University; Victoria, BC Canada
1
Key words: Nepenthes, tree shrew, nitrogen sequestration, mutualism, animal-plant interactions
Three species of Nepenthes pitcher plants from Borneo engage in a mutualistic interaction with mountain tree shrews, the basis of which is the exchange of nutritional resources. The plants produce modified “toilet pitchers” that produce copious amounts of exudates, the latter serving as a food source for tree shrews. The exudates are only accessible to the tree shrews when they position their hindquarters over the pitcher orifice. Tree shrews mark valuable resources with feces and regularly defecate into the pitchers when they visit them to feed. Feces represent a valuable source of nitrogen for these Nepenthes species, but there are many facets of the mutualism that are yet to be investigated. These include, but are not limited to, seasonal variation in exudate production rates by the plants, behavioral ecology of visiting tree shrews and the mechanism by which the plants signal to tree shrews that their pitchers represent a food source. Further research into this extraordinary animalplant interaction is required to gain a better understanding of the benefits to the participating species.
The pitcher plant genus Nepenthes comprises approximately 120 species, with the centre of diversity lying in the perhumid tropics of Southeast Asia. All species are vines or subscandent shrubs that produce highly modified leaf organs (“pitchers”) which typically attract, trap, retain and digest arthropods for nutritional benefit. The pitchers of almost all Nepenthes species share the same physical components,1 including the pitcher cup, the peristome and the lid. The pitcher cup usually consists of two main sections: an upper zone which is often covered with wax crystals and anisotropically-oriented semilunate cells2,3 that assist in the capture and retention of prey; and a lower portion, which contains fluid and is lined with digestive glands.2,3 The peristome is a ridge of hardened tissue that lines the orifice. Its anisotropic, wettable surface plays a key role in prey capture.4,5 In most species, the lid is a broad, flat structure which overhangs the orifice and prevents the entry of rainwater which, if unimpeded, can *Correspondence to: Charles Clarke; Email: [email protected] Submitted: 06/22/10; Accepted: 06/28/10 Previously published online: www.landesbioscience.com/journals/psb/article/12807 DOI: 10.4161/psb.5.10.12807
www.landesbioscience.com
cause the pitchers to overflow, thereby losing digestive enzymes and the products of their activities. The lid is often brightly coloured, has many nectar glands on its surfaces and plays an important role in prey attraction.2 The degree of development and/or modification of each pitcher component varies substantially among (and even within) Nepenthes species2,6,7 and recent research has demonstrated that unique modifications to pitcher structure possessed by several species play important roles in specialized nutrient acquisition strategies.8-12 One such species, Nepenthes lowii, demonstrates a remarkable nitrogen sequestration strategy, in which mountain tree shrews (Tupaia montana) defecate into its pitchers while feeding on exudates secreted by glands on the inner surface of the pitcher lid. Feces accounts for 57–100% of foliar nitrogen in this species13 and N. lowii “toilet pitchers” are ineffective arthropod traps. The large orifices and reflexed, concave lids of N. lowii pitchers induce T. montana to sit astride the pitcher whilst feeding, facilitating fecal deposition. Chin et al.14 found that two other montane species from Borneo, Nepenthes rajah and Nepenthes macrophylla, also trap tree shrew feces. Detailed analysis of trap geometry revealed that these two species and N. lowii share a unique arrangement of trap characteristics that was not detected by earlier studies on the genus. This involves the production of pitchers with very large orifices, large, concave lids that are reflexed approximately 90° away from the orifice and lid glands that produce copious exudates.14 The distance from the front of the pitcher orifice to the inner surface of the lid precisely matches the head + body length of T. montana, resulting in the tree shrews’ food source being positioned behind the pitcher orifice and ensuring that the animals’ hindquarters are positioned over the orifice while they feed on the lid gland exudates. Thus, N. lowii, N. macrophylla and N. rajah are all engaged in a mutualism with T. montana, the basis of which is the exchange of nutritional resources that are scarce in these species’ habitats. The interaction with T. montana is facilitated by trap geometry, but all three Nepenthes species produce pitchers that differ substantially in structure, apart from the shared characteristics outlined above.14 Through a series of modifications to trap structure and geometry—none of which appears to have compromised their ability to trap arthropod prey—N. rajah and N. macrophylla
Plant Signaling & Behavior
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benefit from a highly specialised nitrogen sequestration strategy that is not available to congeners other than N. lowii. Although Clarke et al.13 demonstrated that N. lowii derives nutritional benefit from T. montana feces, there are many facets of the association that have yet to be investigated and the discoveries of Chin et al.14 give rise to a number avenues for further research, several of which are discussed below. The behavioral ecology of T. montana with respect to Nepenthes has not been studied in detail. We do not know whether individual tree shrews defend valuable pitchers against other animals or whether such resources are shared. However, video footage, showing T. montana scent-marking a toilet pitcher of N. lowii after feeding from it, supports the former scenario (Clarke et al.13 and Suppl. video). It is not known whether or how, the plants signal to tree shrews that their pitchers provide a nutritional resource (or even how valuable that resource is—the composition and nutritional value of the lid gland exudates has not been determined). When newly-formed pitchers first open, their tissues generally remain soft for several days while they undergo rapid expansion during the final stages of development.1 During this period, the pitchers are incapable of supporting a tree shrew without suffering significant damage, yet few pitchers of N. lowii, N. macrophylla or N. rajah that we observed exhibited signs of such damage. One possible explanation for this is that the plants signal the tree shrews to indicate whether or not individual pitchers are “open for business.” This might be achieved using variations in color: Tupaia spp. are dichromatic, with sensitivity maxima at ca. 440 and 550–560 nm15 and the pitchers of all three feces-trapping Nepenthes species utilize combinations of green, red, yellow, orange and purple pigments, which change as individual pitchers age.1 In N. lowii, the inner surfaces of the feces-trapping pitchers are uniformly dark purple when mature, but when they first open, they are unevenly covered with purple, pink and green patches. The production of copious lid gland exudates in N. lowii appears to commence after the pitchers have hardened and the uniform dark purple color has developed on the inner surfaces. The study by Chin et al.14 was based on a series of three field trips to northern Borneo that were conducted in March, April and May 2009. The first of these two visits took place during the wet season and heavy rain fell on most days throughout these months. In contrast, May was unusually dry. During this period, many N. rajah plants exhibited signs of stress due to lack of water, including wilting or senescence of developing pitchers and inflorescences. This coincided with an apparent (but unquantified) decline in the number of pitchers that received tree shrew feces: whereas such pitchers were relatively easy to locate during our visits in March and April, they were rare during May. Furthermore, most pitchers that received copious amounts of feces in March and April received none in May. The reasons for this are unknown and may involve changes in the foraging behaviour of T. montana or perhaps a reduction in the quantity and/or quality of the lid gland secretions. Through video recordings, we found that
1188
T. montana still visited pitchers of N. rajah during May (Chin et al.14), but very few fecal pellets were deposited inside them. Tree shrews mark valuable resources using feces,16 so it is feasible that during periods of decreased nectar production, T. montana alters its foraging behavior to utilize alternative food resources, resulting in decreased rates of defecation into N. rajah pitchers. N. lowii, N. rajah and N. macrophylla are virtually confined to montane habitats above 1,800 m altitude, but the geographical range of T. montana extends well beyond that of the “toilet pitchers” and includes a number of sites that are substantially lower than 1,800 m.17 Given this, why are the toilet pitchers not found at lower altitudes? Large, fleshy fruits with small seeds (such as figs) comprise a major component of the diet of T. montana,18 but plants that produce these are relatively scarce in alpine and upper montane equatorial habitats.19 This could limit the distribution of toilet pitchers in two ways. First, the lack of fleshy fruits at high altitudes might make toilet pitchers a valuable resource for T. montana in upper montane habitats. Furthermore, the density of arthropods at high altitudes is considerably less than in the lowlands.20 This exerts selective pressure on Nepenthes to adopt non-carnivorous nutrient acquisition strategies.13 Accordingly, the production of very large, specialized pitchers that receive a steady input of feces may provide a net benefit for the plants, but only at high altitudes. Second, at lower altitudes, fleshy fruits (and arthropods) are more abundant and at these sites the benefits of producing toilet pitchers may be reduced or even negated, hence their absence from smaller mountains. Through their unique pitcher characteristics and trap geometries, a number of Nepenthes species derive supplementary nutrition from a wide variety of arthropod groups, leaf litter and animal feces.6,10,13,14,21,22 It is arguable that no other plant family has such a complex and diverse array of interactions with animals. Recent discoveries add to a growing body of evidence to suggest that Nepenthes demonstrate adaptive radiation with regard to nutrient sequestration strategies (see Chin et al.14 for a more detailed discussion). The findings of Chin et al.14 provide the strongest support for this hypothesis to date; in addition, they provide the first plausible explanation for the extraordinary size of N. rajah pitchers. This iconic species is the world’s largest carnivorous plant and was first described 150 years ago. The population studied by Chin et al.14 grows at a site on Mount Kinabalu that has been visited by tourists since 2001 and has been regularly examined by scientists and Sabah Parks staff for more than 30 years. Despite this, the association between N. rajah and T. montana remained undetected until we employed remote survey methods to record pitcher visitors. To date, this technique has been used on just five species of Nepenthes4,5,13,14 and in each case, remarkable insights into the interactions between animals and Nepenthes have been gained. The potential for further discoveries using this method is therefore high and through new and innovative experimental methodologies now being employed, we anticipate many more exciting discoveries in the near future.
Plant Signaling & Behavior Volume 5 Issue 10
References 1. Clarke CM. Nepenthes of Borneo. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 1997. 2. Lloyd FE. The carnivorous plants. New York, NY USA: Chronica Botanica 1942. 3. Juniper BE, Robins RJ, Joel D. The carnivorous plants. London UK: Academic Press 1989. 4. Bonn HF, Federle W. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proc Natl Acad Sci USA 2004; 101:14138-43. 5. Bauer U, Bohn HF, Federle W. Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proc Royal Society B 2008; 275:259-65. 6. Clarke CM. Nepenthes of Sumatra & Peninsular Malaysia. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 2001. 7. Phillipps A, Lamb A, Lee CC. Pitcher plants of Borneo, 2nd edn. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 2009. 8. Clarke CM, Kitching RL. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. J Trop Ecol 1995; 11:589-602.
www.landesbioscience.com
9.
10.
11.
12.
13.
14.
Moran JA, Merbach MA, Livingston NJ, Clarke CM, Booth WE. Termite prey specialization in the pitcher plant Nepenthes albomarginata—evidence from stable isotope analysis. Ann Bot 2001; 88:307-11. Moran JA, Clarke CM, Hawkins BJ. From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. Int J Plant Sci 2003; 164:635-9. Merbach MA, Merbach DJ, Maschwitz U, Booth WE, Fiala B, Zizka G. Mass march of termites into the deadly trap. Nature 2002; 415:37. Merbach MA, Zizka G, Fiala B, Merbach D, Booth WE, Maschwitz U. Why a carnivorous plant cooperates with an ant—selective defense against pitcher-destroying weevils in the myrmecophytic pitcher plant Nepenthes bicalcarata Hook.f. Ecotropica 2007; 13:45-56. Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA. Tree shrew lavatories: a novel nitrogen sequestration strategy in tropical pitcher plants. Biol Lett 2009: 5:632-5. Chin L, Moran JA, Clarke C. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytol 2010; 186:461-70.
15. Jacobs GH, Neitz J. Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri). Vision Res 1986; 26:291-8. 16. Kawamichi T, Kawamichi M. Spatial organization and territory in tree shrews (Tupaia glis). Anim Behav 1979; 27:381-93. 17. Payne J, Francis CM, Phillipps K. A field guide to the mammals of Borneo. Kota Kinabalu, Malaysia: Sabah Society 1985. 18. Emmons LH. Frugivory in treeshrews (Tupaia). Am Nat 1991; 138:642-9. 19. Smith AP. Tropical Alpine Plant Ecology. Ann Rev Ecol Syst 1987; 18:137-58. 20. Collins NM. The distribution of soil macrofauna on the west ridge of Gunung (Mount) Mulu, Sarawak. Oecologia 1980; 44:263-75. 21. Kato M, Hotta M, Tamin R, Itino T. Inter- and Intraspecific variation in prey assemblages and inhabitant communities in Nepenthes pitchers in Sumatra. Tropical Zoology 1993; 6:11-25. 22. Moran JA. Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. J Ecol 1996; 84:515-25.
Plant Signaling & Behavior 1189
Mini-Review
Plant Signaling & Behavior 5:10, 1187-1189; October 2010; © 2010 Landes Bioscience
Mutualism between tree shrews and pitcher plants
Perspectives and avenues for future research Charles Clarke,1,* Jonathan A. Moran2 and Lijin Chin1 School of Science; Monash University Sunway Campus; Bandar Sunway; Selangor, Malaysia; 2School of Environment and Sustainability; Royal Roads University; Victoria, BC Canada
1
Key words: Nepenthes, tree shrew, nitrogen sequestration, mutualism, animal-plant interactions
Three species of Nepenthes pitcher plants from Borneo engage in a mutualistic interaction with mountain tree shrews, the basis of which is the exchange of nutritional resources. The plants produce modified “toilet pitchers” that produce copious amounts of exudates, the latter serving as a food source for tree shrews. The exudates are only accessible to the tree shrews when they position their hindquarters over the pitcher orifice. Tree shrews mark valuable resources with feces and regularly defecate into the pitchers when they visit them to feed. Feces represent a valuable source of nitrogen for these Nepenthes species, but there are many facets of the mutualism that are yet to be investigated. These include, but are not limited to, seasonal variation in exudate production rates by the plants, behavioral ecology of visiting tree shrews and the mechanism by which the plants signal to tree shrews that their pitchers represent a food source. Further research into this extraordinary animalplant interaction is required to gain a better understanding of the benefits to the participating species.
The pitcher plant genus Nepenthes comprises approximately 120 species, with the centre of diversity lying in the perhumid tropics of Southeast Asia. All species are vines or subscandent shrubs that produce highly modified leaf organs (“pitchers”) which typically attract, trap, retain and digest arthropods for nutritional benefit. The pitchers of almost all Nepenthes species share the same physical components,1 including the pitcher cup, the peristome and the lid. The pitcher cup usually consists of two main sections: an upper zone which is often covered with wax crystals and anisotropically-oriented semilunate cells2,3 that assist in the capture and retention of prey; and a lower portion, which contains fluid and is lined with digestive glands.2,3 The peristome is a ridge of hardened tissue that lines the orifice. Its anisotropic, wettable surface plays a key role in prey capture.4,5 In most species, the lid is a broad, flat structure which overhangs the orifice and prevents the entry of rainwater which, if unimpeded, can *Correspondence to: Charles Clarke; Email: [email protected] Submitted: 06/22/10; Accepted: 06/28/10 Previously published online: www.landesbioscience.com/journals/psb/article/12807 DOI: 10.4161/psb.5.10.12807
www.landesbioscience.com
cause the pitchers to overflow, thereby losing digestive enzymes and the products of their activities. The lid is often brightly coloured, has many nectar glands on its surfaces and plays an important role in prey attraction.2 The degree of development and/or modification of each pitcher component varies substantially among (and even within) Nepenthes species2,6,7 and recent research has demonstrated that unique modifications to pitcher structure possessed by several species play important roles in specialized nutrient acquisition strategies.8-12 One such species, Nepenthes lowii, demonstrates a remarkable nitrogen sequestration strategy, in which mountain tree shrews (Tupaia montana) defecate into its pitchers while feeding on exudates secreted by glands on the inner surface of the pitcher lid. Feces accounts for 57–100% of foliar nitrogen in this species13 and N. lowii “toilet pitchers” are ineffective arthropod traps. The large orifices and reflexed, concave lids of N. lowii pitchers induce T. montana to sit astride the pitcher whilst feeding, facilitating fecal deposition. Chin et al.14 found that two other montane species from Borneo, Nepenthes rajah and Nepenthes macrophylla, also trap tree shrew feces. Detailed analysis of trap geometry revealed that these two species and N. lowii share a unique arrangement of trap characteristics that was not detected by earlier studies on the genus. This involves the production of pitchers with very large orifices, large, concave lids that are reflexed approximately 90° away from the orifice and lid glands that produce copious exudates.14 The distance from the front of the pitcher orifice to the inner surface of the lid precisely matches the head + body length of T. montana, resulting in the tree shrews’ food source being positioned behind the pitcher orifice and ensuring that the animals’ hindquarters are positioned over the orifice while they feed on the lid gland exudates. Thus, N. lowii, N. macrophylla and N. rajah are all engaged in a mutualism with T. montana, the basis of which is the exchange of nutritional resources that are scarce in these species’ habitats. The interaction with T. montana is facilitated by trap geometry, but all three Nepenthes species produce pitchers that differ substantially in structure, apart from the shared characteristics outlined above.14 Through a series of modifications to trap structure and geometry—none of which appears to have compromised their ability to trap arthropod prey—N. rajah and N. macrophylla
Plant Signaling & Behavior
1187
benefit from a highly specialised nitrogen sequestration strategy that is not available to congeners other than N. lowii. Although Clarke et al.13 demonstrated that N. lowii derives nutritional benefit from T. montana feces, there are many facets of the association that have yet to be investigated and the discoveries of Chin et al.14 give rise to a number avenues for further research, several of which are discussed below. The behavioral ecology of T. montana with respect to Nepenthes has not been studied in detail. We do not know whether individual tree shrews defend valuable pitchers against other animals or whether such resources are shared. However, video footage, showing T. montana scent-marking a toilet pitcher of N. lowii after feeding from it, supports the former scenario (Clarke et al.13 and Suppl. video). It is not known whether or how, the plants signal to tree shrews that their pitchers provide a nutritional resource (or even how valuable that resource is—the composition and nutritional value of the lid gland exudates has not been determined). When newly-formed pitchers first open, their tissues generally remain soft for several days while they undergo rapid expansion during the final stages of development.1 During this period, the pitchers are incapable of supporting a tree shrew without suffering significant damage, yet few pitchers of N. lowii, N. macrophylla or N. rajah that we observed exhibited signs of such damage. One possible explanation for this is that the plants signal the tree shrews to indicate whether or not individual pitchers are “open for business.” This might be achieved using variations in color: Tupaia spp. are dichromatic, with sensitivity maxima at ca. 440 and 550–560 nm15 and the pitchers of all three feces-trapping Nepenthes species utilize combinations of green, red, yellow, orange and purple pigments, which change as individual pitchers age.1 In N. lowii, the inner surfaces of the feces-trapping pitchers are uniformly dark purple when mature, but when they first open, they are unevenly covered with purple, pink and green patches. The production of copious lid gland exudates in N. lowii appears to commence after the pitchers have hardened and the uniform dark purple color has developed on the inner surfaces. The study by Chin et al.14 was based on a series of three field trips to northern Borneo that were conducted in March, April and May 2009. The first of these two visits took place during the wet season and heavy rain fell on most days throughout these months. In contrast, May was unusually dry. During this period, many N. rajah plants exhibited signs of stress due to lack of water, including wilting or senescence of developing pitchers and inflorescences. This coincided with an apparent (but unquantified) decline in the number of pitchers that received tree shrew feces: whereas such pitchers were relatively easy to locate during our visits in March and April, they were rare during May. Furthermore, most pitchers that received copious amounts of feces in March and April received none in May. The reasons for this are unknown and may involve changes in the foraging behaviour of T. montana or perhaps a reduction in the quantity and/or quality of the lid gland secretions. Through video recordings, we found that
1188
T. montana still visited pitchers of N. rajah during May (Chin et al.14), but very few fecal pellets were deposited inside them. Tree shrews mark valuable resources using feces,16 so it is feasible that during periods of decreased nectar production, T. montana alters its foraging behavior to utilize alternative food resources, resulting in decreased rates of defecation into N. rajah pitchers. N. lowii, N. rajah and N. macrophylla are virtually confined to montane habitats above 1,800 m altitude, but the geographical range of T. montana extends well beyond that of the “toilet pitchers” and includes a number of sites that are substantially lower than 1,800 m.17 Given this, why are the toilet pitchers not found at lower altitudes? Large, fleshy fruits with small seeds (such as figs) comprise a major component of the diet of T. montana,18 but plants that produce these are relatively scarce in alpine and upper montane equatorial habitats.19 This could limit the distribution of toilet pitchers in two ways. First, the lack of fleshy fruits at high altitudes might make toilet pitchers a valuable resource for T. montana in upper montane habitats. Furthermore, the density of arthropods at high altitudes is considerably less than in the lowlands.20 This exerts selective pressure on Nepenthes to adopt non-carnivorous nutrient acquisition strategies.13 Accordingly, the production of very large, specialized pitchers that receive a steady input of feces may provide a net benefit for the plants, but only at high altitudes. Second, at lower altitudes, fleshy fruits (and arthropods) are more abundant and at these sites the benefits of producing toilet pitchers may be reduced or even negated, hence their absence from smaller mountains. Through their unique pitcher characteristics and trap geometries, a number of Nepenthes species derive supplementary nutrition from a wide variety of arthropod groups, leaf litter and animal feces.6,10,13,14,21,22 It is arguable that no other plant family has such a complex and diverse array of interactions with animals. Recent discoveries add to a growing body of evidence to suggest that Nepenthes demonstrate adaptive radiation with regard to nutrient sequestration strategies (see Chin et al.14 for a more detailed discussion). The findings of Chin et al.14 provide the strongest support for this hypothesis to date; in addition, they provide the first plausible explanation for the extraordinary size of N. rajah pitchers. This iconic species is the world’s largest carnivorous plant and was first described 150 years ago. The population studied by Chin et al.14 grows at a site on Mount Kinabalu that has been visited by tourists since 2001 and has been regularly examined by scientists and Sabah Parks staff for more than 30 years. Despite this, the association between N. rajah and T. montana remained undetected until we employed remote survey methods to record pitcher visitors. To date, this technique has been used on just five species of Nepenthes4,5,13,14 and in each case, remarkable insights into the interactions between animals and Nepenthes have been gained. The potential for further discoveries using this method is therefore high and through new and innovative experimental methodologies now being employed, we anticipate many more exciting discoveries in the near future.
Plant Signaling & Behavior Volume 5 Issue 10
References 1. Clarke CM. Nepenthes of Borneo. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 1997. 2. Lloyd FE. The carnivorous plants. New York, NY USA: Chronica Botanica 1942. 3. Juniper BE, Robins RJ, Joel D. The carnivorous plants. London UK: Academic Press 1989. 4. Bonn HF, Federle W. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proc Natl Acad Sci USA 2004; 101:14138-43. 5. Bauer U, Bohn HF, Federle W. Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proc Royal Society B 2008; 275:259-65. 6. Clarke CM. Nepenthes of Sumatra & Peninsular Malaysia. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 2001. 7. Phillipps A, Lamb A, Lee CC. Pitcher plants of Borneo, 2nd edn. Kota Kinabalu, Sabah, Malaysia: Natural History Publications (Borneo) 2009. 8. Clarke CM, Kitching RL. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. J Trop Ecol 1995; 11:589-602.
www.landesbioscience.com
9.
10.
11.
12.
13.
14.
Moran JA, Merbach MA, Livingston NJ, Clarke CM, Booth WE. Termite prey specialization in the pitcher plant Nepenthes albomarginata—evidence from stable isotope analysis. Ann Bot 2001; 88:307-11. Moran JA, Clarke CM, Hawkins BJ. From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. Int J Plant Sci 2003; 164:635-9. Merbach MA, Merbach DJ, Maschwitz U, Booth WE, Fiala B, Zizka G. Mass march of termites into the deadly trap. Nature 2002; 415:37. Merbach MA, Zizka G, Fiala B, Merbach D, Booth WE, Maschwitz U. Why a carnivorous plant cooperates with an ant—selective defense against pitcher-destroying weevils in the myrmecophytic pitcher plant Nepenthes bicalcarata Hook.f. Ecotropica 2007; 13:45-56. Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA. Tree shrew lavatories: a novel nitrogen sequestration strategy in tropical pitcher plants. Biol Lett 2009: 5:632-5. Chin L, Moran JA, Clarke C. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytol 2010; 186:461-70.
15. Jacobs GH, Neitz J. Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri). Vision Res 1986; 26:291-8. 16. Kawamichi T, Kawamichi M. Spatial organization and territory in tree shrews (Tupaia glis). Anim Behav 1979; 27:381-93. 17. Payne J, Francis CM, Phillipps K. A field guide to the mammals of Borneo. Kota Kinabalu, Malaysia: Sabah Society 1985. 18. Emmons LH. Frugivory in treeshrews (Tupaia). Am Nat 1991; 138:642-9. 19. Smith AP. Tropical Alpine Plant Ecology. Ann Rev Ecol Syst 1987; 18:137-58. 20. Collins NM. The distribution of soil macrofauna on the west ridge of Gunung (Mount) Mulu, Sarawak. Oecologia 1980; 44:263-75. 21. Kato M, Hotta M, Tamin R, Itino T. Inter- and Intraspecific variation in prey assemblages and inhabitant communities in Nepenthes pitchers in Sumatra. Tropical Zoology 1993; 6:11-25. 22. Moran JA. Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. J Ecol 1996; 84:515-25.
Plant Signaling & Behavior 1189
