Abstract
A new endemic species, Nepenthes candalaga (Nepenthes sect. Alata) from Mt. Candalaga (eastern Mindanao, Philippines) is here described and illustrated. This new taxon resembles N. justinae but can be easily distinguished in having the lamina with 2‒3 longitudinal nerves, orbicular lid, non-bifid lid spur tip, triangular lid appendage, short banner-shaped trap wings, and absent upper pitcher rim. The species is assessed as Critically Endangered (CE) according to the IUCN criteria. This novelty is the 38th species of Nepenthes in Mindanao making the island with the highest concentration of Nepenthes species in the Philippines. This discovery increases the number of Nepenthes species in the Philippines to 61. The new taxon described faces threats of deforestation and habitat loss without legislative protection.
References
Bauer, U., Bohn, H.F. & Federle, W. (2007) Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proceedings of the Royal Society B, Biological Sciences 275 (1632): 259–265. https://doi.org/10.1098/rspb.2007.1402
Bauer, U., Di Giusto, B., Skepper, J., Grafe, T.U. & Federle, W. (2012) With a flick of the lid: A novel trapping mechanism in Nepenthes gracilis pitcher plants. PLoSOne 7: 1–7. https://doi.org/10.1371/journal.pone.0038951
Bazile, V. Moguédec, G. Le, Marshall, D.J. & Gaume, L. (2015) Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Annals of Botany 115: 705–716. https://doi.org/10.1093/aob/mcu266
Blanco, F.M. (1837) Nepenthes. Flora de Filipinas. Santo Thomas [printers] por D. Candido Lopez, Manila, 619 pp.
Briones, N.D. (2007) Environmental sustainability issues in Philippine agriculture. Asian Journal of Agriculture and Development 2: 67–78.
Chase, M.W., Christenhusz, M.J.M., Sanders, D. & Fay, M.F. (2009) Murderous plants: Victoraian Gothic, Darwin and modern insights into vegetable carnivory. Botanical Journal of the Linnean Society 161 (4): 329–356. https://doi.org/10.1111/j.1095-8339.2009.01014.x
Cheek, M.R. & Jebb, M.H.P. (2001) Flora Malesiana. Series I – Seed plants, vol. 15: Nepenthaceae. Nationaal Herbarium Nederland, Leiden, iv + 164 pp.
Cheek, M. & Jebb, M. (2013) Recircumscription of the Nepenthes alata group (Caryophyllales: Nepenthaceae), in the Philippines, with four new species. European Journal of Taxonomy 69: 1–23. https://doi.org/10.5852/ejt.2013.69
Cheek, M., Jebb, M. & Murphy, B. (2019) A classification of functional pitcher types in Nepenthes (Nepenthaceae). Biorxiv (preprint) https://doi.org/10.1101/852137
Clarke, C.M. (2001) Nepenthes of Sumatra and Peninsular Malaysia. Natural History Publications (Borneo), Kota Kinabalu, x + 326 pp.
Clarke, S.J. & Robinson, A.S. (2018) Species of carnivorous plants. In: Ellison, A.M. & Adamec, L. (Eds.) Carnivorous Plants: Physiology, Ecology, and Evolution. Oxford University Press, Oxford, pp. 411–413.
Clarke, C., Bauer, U., Lee, C.C., Tuen, A.A., Rembold, K. & Moran, J.A. (2009) Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5: 632–635. https://doi.org/10.1098/rsbl.2009.0311
Coritico, F.P., Lagunday, N.E., Galindon, J.M., Tandang, D.N. & Amoroso, V.B. (2020) Diversity of trees and structure of forest habitat types in Mt. Tago Range, Mindanao, Philippines. Philippine Journal of Systematic Biology 14 (3): 1–11. https://doi.org/10.26757/pjsb2020c14006
Danser, B.H. (1928) The Nepenthaceae of the Netherlands Indies. Bulletin du Jardin de Botanique de Buitenzorg, Série III 9: 249–438.
Darwin, C. (1875) Insectivorous Plants. John Murray, London, 476 pp. https://doi.org/10.5962/bhl.title.99933
Ellison, A.M. & Adamec, L. (2018) Carnivorous Plants: Physiology, Ecology and Evolution. Oxford University Press, Oxford, 509 pp. https://doi.org/10.1093/oso/9780198779841.001.0001
Fukushima, K., Fang, X., Alvarez-Ponce, D., Cai, H., Carretero-Paulet, L., Chen, C., Chang, T.-H., Farr, K.M., Fujita, T., Hiwatashi, Y., Hoshi, Y., Imai, T., Kasahara, M., Librado, P., Mao, L., Mori, H., Nishiyama, T., Nozawa, M., Pálfalvi, G., Pollard, S.T., Rozas, J., Sánchez-Gracia, A., Sankoff, D., Shibata, T.F., Shigenobu, S., Sumikawa, N., Uzawa, T., Xie, M., Zheng, C., Pollock, D.D., Albert, V.A., Li, S. & Hasebe, M. (2017) Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nature Ecology & Evolution 1 (0059): 1–9. https://doi.org/10.1038/s41559-016-0059
Gaume, L., Gorb, S. & Rowe, N. (2017) Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. New Phytologist 156: 479–489. https://doi.org/10.1046/j.1469-8137.2002.00530.x
Gronemeyer, T., Suarez, W., Nuytemans, H., Calaramo, M., Wistuba, A., Mey, F.S. & Amoroso, V.B. (2016) Two new Nepenthes species from the Philippines and an emended description of Nepenthes ramos. Plants 5: 1–15. https://doi.org/10.3390/plants5020023
IUCN Standards and Petitions Committee (2022) Guidelines for Using the IUCN Red List Categories and Criteria. Version 15. Prepared by the Standards and Petitions Committee. Available from: https://www.iucnredlist.org/documents/RedListGuidelines.pdf (accessed 17 May 2022)
Jebb, M. & Cheek, M. (1997) A skeletal revision of Nepenthes (Nepenthaceae). Blumea Journal of Plant Taxonomy and Plant Geography 42: 1–106.
Juniper, B. & Joel, D.M. (1989) The Carnivorous Plants. Academic Press Ltd., London, 353 pp.
King, C. & Cheek, M. (2020) Nepenthes maximoides (Nepenthaceae) a new, critically endangered (possibly extinct) species in Sect. Alatae from Luzon, Philippines showing striking pitcher convergence with N. maxima (Sect. Regiae) of Indonesia. PeerJ 8: e9899. https://doi.org/10.7717/peerj.9899
Lim, Y.S., Schöner, M.G., Kerth, G., Thornham, D.G., Scharmann, M. & Grafe, T.U. (2014) How a pitcher plant facilitates roosting of a mutualistic woolly bats. Evolutionary Ecology Research 16: 581–591.
Mansell, G. & Suarez, W. (2016) Nepenthes nebularum, a new species from Mindanao, Philippines. Carnivorous Plant Newsletter 45: 132–139. https://doi.org/10.55360/cpn454.gm291
McPherson, S.R. (2009) Pitcher plants of the Old World, vols. 1–2. Redfern Natural History Productions, Poole, 1399 pp.
Merbach, M.A., Merbach, D.J., Maschwitz, U., Booth, W.E., Fiala, B. & Zizka, G. (2002) Mass march of termites into the deadly trap. Nature 415: 36–37. https://doi.org/10.1038/415036a
Moran, J.A., Clarke, C. & Gowen, B.E. (2012) The use of light in prey capture by the tropical pitcher plant Nepenthes aristolochioides. Plant Signaling & Behavior 7: 957–960. https://doi.org/10.4161/psb.20912
Moya, T.B. & Malayang, B.S. (2004) Climate variability and deforestation-reforestation dynamics in the Philippines. Environment, Development and Sustainability 6: 261–277. https://doi.org/10.1023/B:ENVI.0000003640.97351.92
Murphy, B., Forest, F., Barraclough, T., Rosindell, J., Bellot, S., Cowan, S., Golos, M., Jebb, M. & Cheek, M. (2020) A phylogenomic analysis of Nepenthes (Nepenthaceae). Molecular Phylogenetics and Evolution 144: 106668. https://doi.org/10.1016/j.ympev.2019.106668
Pavlovi?, A., Slováková, ?. & Šantr??ek, J. (2011) Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria. Plant, Cell Environ 34: 1865–1873. https://doi.org/10.1111/j.1365-3040.2011.02382.x
Posa, M.R.C. & Sodhi, N.S. (2006) Effects of anthropogenic land use on forest birds and butterflies in Subic Bay, Philippines. Biological Conservation 129: 256–270. https://doi.org/10.1016/j.biocon.2005.10.041
Robinson, A.S., Fleischmann, A.S., McPherson, S.R., Heinrich, V.B., Gironella, E.P. & Peña, C.Q. (2009) A spectacular new species of Nepenthes L. (Nepenthaceae) pitcher plant from central Palawan, Philippines. Botanical Journal of the Linnean Society 159 (2): 195–202. https://doi.org/10.1111/j.1095-8339.2008.00942.x
Scharmann, M., Thornham, D.G., Grafe, T.U. & Federle, W. (2013) A novel type of nutritional ant-plant interaction: Ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna. PLoS One 8 (5): e63556. https://doi.org/10.1371/journal.pone.0063556
Sholz, I., Bückins, M., Dolge, L., Erlinghagen, T., Weth, A., Hischen, F., Mayer, J., Hoffmann, S., Riederer, M., Riedel, M. & Baumgartner, W. (2010) Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. Journal of Experimental Biology 213: 1115–1125. https://doi.org/10.1242/jeb.035618
Tandang, D.N., Galindon, J.M.M., Lagunday, N.E., Coritico, F.P., Amoroso, V.B. & Robinson, A.S. (2021) Amylotheca cleofei sp. nov. (Loranthaceae), a new species and genus record for the Philippines. Phytotaxa 507 (1): 113–120. https://doi.org/10.11646/phytotaxa.507.1.7
Thorogood, C.J., Bauer, U. & Hiscock, S.J. (2018) Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytologist 217: 1035–1041. https://doi.org/10.1111/nph.14879
Bauer, U., Di Giusto, B., Skepper, J., Grafe, T.U. & Federle, W. (2012) With a flick of the lid: A novel trapping mechanism in Nepenthes gracilis pitcher plants. PLoSOne 7: 1–7. https://doi.org/10.1371/journal.pone.0038951
Bazile, V. Moguédec, G. Le, Marshall, D.J. & Gaume, L. (2015) Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Annals of Botany 115: 705–716. https://doi.org/10.1093/aob/mcu266
Blanco, F.M. (1837) Nepenthes. Flora de Filipinas. Santo Thomas [printers] por D. Candido Lopez, Manila, 619 pp.
Briones, N.D. (2007) Environmental sustainability issues in Philippine agriculture. Asian Journal of Agriculture and Development 2: 67–78.
Chase, M.W., Christenhusz, M.J.M., Sanders, D. & Fay, M.F. (2009) Murderous plants: Victoraian Gothic, Darwin and modern insights into vegetable carnivory. Botanical Journal of the Linnean Society 161 (4): 329–356. https://doi.org/10.1111/j.1095-8339.2009.01014.x
Cheek, M.R. & Jebb, M.H.P. (2001) Flora Malesiana. Series I – Seed plants, vol. 15: Nepenthaceae. Nationaal Herbarium Nederland, Leiden, iv + 164 pp.
Cheek, M. & Jebb, M. (2013) Recircumscription of the Nepenthes alata group (Caryophyllales: Nepenthaceae), in the Philippines, with four new species. European Journal of Taxonomy 69: 1–23. https://doi.org/10.5852/ejt.2013.69
Cheek, M., Jebb, M. & Murphy, B. (2019) A classification of functional pitcher types in Nepenthes (Nepenthaceae). Biorxiv (preprint) https://doi.org/10.1101/852137
Clarke, C.M. (2001) Nepenthes of Sumatra and Peninsular Malaysia. Natural History Publications (Borneo), Kota Kinabalu, x + 326 pp.
Clarke, S.J. & Robinson, A.S. (2018) Species of carnivorous plants. In: Ellison, A.M. & Adamec, L. (Eds.) Carnivorous Plants: Physiology, Ecology, and Evolution. Oxford University Press, Oxford, pp. 411–413.
Clarke, C., Bauer, U., Lee, C.C., Tuen, A.A., Rembold, K. & Moran, J.A. (2009) Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5: 632–635. https://doi.org/10.1098/rsbl.2009.0311
Coritico, F.P., Lagunday, N.E., Galindon, J.M., Tandang, D.N. & Amoroso, V.B. (2020) Diversity of trees and structure of forest habitat types in Mt. Tago Range, Mindanao, Philippines. Philippine Journal of Systematic Biology 14 (3): 1–11. https://doi.org/10.26757/pjsb2020c14006
Danser, B.H. (1928) The Nepenthaceae of the Netherlands Indies. Bulletin du Jardin de Botanique de Buitenzorg, Série III 9: 249–438.
Darwin, C. (1875) Insectivorous Plants. John Murray, London, 476 pp. https://doi.org/10.5962/bhl.title.99933
Ellison, A.M. & Adamec, L. (2018) Carnivorous Plants: Physiology, Ecology and Evolution. Oxford University Press, Oxford, 509 pp. https://doi.org/10.1093/oso/9780198779841.001.0001
Fukushima, K., Fang, X., Alvarez-Ponce, D., Cai, H., Carretero-Paulet, L., Chen, C., Chang, T.-H., Farr, K.M., Fujita, T., Hiwatashi, Y., Hoshi, Y., Imai, T., Kasahara, M., Librado, P., Mao, L., Mori, H., Nishiyama, T., Nozawa, M., Pálfalvi, G., Pollard, S.T., Rozas, J., Sánchez-Gracia, A., Sankoff, D., Shibata, T.F., Shigenobu, S., Sumikawa, N., Uzawa, T., Xie, M., Zheng, C., Pollock, D.D., Albert, V.A., Li, S. & Hasebe, M. (2017) Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nature Ecology & Evolution 1 (0059): 1–9. https://doi.org/10.1038/s41559-016-0059
Gaume, L., Gorb, S. & Rowe, N. (2017) Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. New Phytologist 156: 479–489. https://doi.org/10.1046/j.1469-8137.2002.00530.x
Gronemeyer, T., Suarez, W., Nuytemans, H., Calaramo, M., Wistuba, A., Mey, F.S. & Amoroso, V.B. (2016) Two new Nepenthes species from the Philippines and an emended description of Nepenthes ramos. Plants 5: 1–15. https://doi.org/10.3390/plants5020023
IUCN Standards and Petitions Committee (2022) Guidelines for Using the IUCN Red List Categories and Criteria. Version 15. Prepared by the Standards and Petitions Committee. Available from: https://www.iucnredlist.org/documents/RedListGuidelines.pdf (accessed 17 May 2022)
Jebb, M. & Cheek, M. (1997) A skeletal revision of Nepenthes (Nepenthaceae). Blumea Journal of Plant Taxonomy and Plant Geography 42: 1–106.
Juniper, B. & Joel, D.M. (1989) The Carnivorous Plants. Academic Press Ltd., London, 353 pp.
King, C. & Cheek, M. (2020) Nepenthes maximoides (Nepenthaceae) a new, critically endangered (possibly extinct) species in Sect. Alatae from Luzon, Philippines showing striking pitcher convergence with N. maxima (Sect. Regiae) of Indonesia. PeerJ 8: e9899. https://doi.org/10.7717/peerj.9899
Lim, Y.S., Schöner, M.G., Kerth, G., Thornham, D.G., Scharmann, M. & Grafe, T.U. (2014) How a pitcher plant facilitates roosting of a mutualistic woolly bats. Evolutionary Ecology Research 16: 581–591.
Mansell, G. & Suarez, W. (2016) Nepenthes nebularum, a new species from Mindanao, Philippines. Carnivorous Plant Newsletter 45: 132–139. https://doi.org/10.55360/cpn454.gm291
McPherson, S.R. (2009) Pitcher plants of the Old World, vols. 1–2. Redfern Natural History Productions, Poole, 1399 pp.
Merbach, M.A., Merbach, D.J., Maschwitz, U., Booth, W.E., Fiala, B. & Zizka, G. (2002) Mass march of termites into the deadly trap. Nature 415: 36–37. https://doi.org/10.1038/415036a
Moran, J.A., Clarke, C. & Gowen, B.E. (2012) The use of light in prey capture by the tropical pitcher plant Nepenthes aristolochioides. Plant Signaling & Behavior 7: 957–960. https://doi.org/10.4161/psb.20912
Moya, T.B. & Malayang, B.S. (2004) Climate variability and deforestation-reforestation dynamics in the Philippines. Environment, Development and Sustainability 6: 261–277. https://doi.org/10.1023/B:ENVI.0000003640.97351.92
Murphy, B., Forest, F., Barraclough, T., Rosindell, J., Bellot, S., Cowan, S., Golos, M., Jebb, M. & Cheek, M. (2020) A phylogenomic analysis of Nepenthes (Nepenthaceae). Molecular Phylogenetics and Evolution 144: 106668. https://doi.org/10.1016/j.ympev.2019.106668
Pavlovi?, A., Slováková, ?. & Šantr??ek, J. (2011) Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria. Plant, Cell Environ 34: 1865–1873. https://doi.org/10.1111/j.1365-3040.2011.02382.x
Posa, M.R.C. & Sodhi, N.S. (2006) Effects of anthropogenic land use on forest birds and butterflies in Subic Bay, Philippines. Biological Conservation 129: 256–270. https://doi.org/10.1016/j.biocon.2005.10.041
Robinson, A.S., Fleischmann, A.S., McPherson, S.R., Heinrich, V.B., Gironella, E.P. & Peña, C.Q. (2009) A spectacular new species of Nepenthes L. (Nepenthaceae) pitcher plant from central Palawan, Philippines. Botanical Journal of the Linnean Society 159 (2): 195–202. https://doi.org/10.1111/j.1095-8339.2008.00942.x
Scharmann, M., Thornham, D.G., Grafe, T.U. & Federle, W. (2013) A novel type of nutritional ant-plant interaction: Ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna. PLoS One 8 (5): e63556. https://doi.org/10.1371/journal.pone.0063556
Sholz, I., Bückins, M., Dolge, L., Erlinghagen, T., Weth, A., Hischen, F., Mayer, J., Hoffmann, S., Riederer, M., Riedel, M. & Baumgartner, W. (2010) Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. Journal of Experimental Biology 213: 1115–1125. https://doi.org/10.1242/jeb.035618
Tandang, D.N., Galindon, J.M.M., Lagunday, N.E., Coritico, F.P., Amoroso, V.B. & Robinson, A.S. (2021) Amylotheca cleofei sp. nov. (Loranthaceae), a new species and genus record for the Philippines. Phytotaxa 507 (1): 113–120. https://doi.org/10.11646/phytotaxa.507.1.7
Thorogood, C.J., Bauer, U. & Hiscock, S.J. (2018) Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytologist 217: 1035–1041. https://doi.org/10.1111/nph.14879