Jump to content

Nepenthes bicalcarata: Difference between revisions

From Wikipedia, the free encyclopedia
Browse history interactively
← Previous editNext edit →
Content deleted Content added
VisualWikitext
updated with refs
Line 17: Line 17:
|}}
|}}


'''''Nepenthes bicalcarata''''' ({{IPAc-en|icon|n|ɨ|ˈ|p|ɛ|n|θ|iː|z|_|b|aɪ|ˌ|k|æ|l|k|ə|ˈ|r|ɑː|t|ə}} or {{IPAc-en|b|ɪ|ˌ|k|æ|l|k|ə|ˈ|r|eɪ|t|ə}}; [[Latin]]: ''bi'' "two", ''calcaratus'' "spur"), also known as the '''Fanged Pitcher-Plant''',<ref name=P&L>Phillipps, A. & A. Lamb 1996. ''[[Pitcher-Plants of Borneo]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref> is a tropical [[pitcher plant]] [[endemism|endemic]] to northwestern [[Borneo]].
'''''Nepenthes bicalcarata''''' ({{IPAc-en|icon|n|ɨ|ˈ|p|ɛ|n|θ|iː|z|_|b|aɪ|ˌ|k|æ|l|k|ə|ˈ|r|ɑː|t|ə}} or {{IPAc-en|b|ɪ|ˌ|k|æ|l|k|ə|ˈ|r|eɪ|t|ə}}; [[Latin]]: ''bi'' "two", ''calcaratus'' "spur"), also known as the '''Fanged Pitcher-Plant''',<ref name=P&L>Phillipps, A. & A. Lamb 1996. ''[[Pitcher-Plants of Borneo]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref> is a tropical [[pitcher plant]] [[endemism|endemic]] to northwestern [[Borneo]]. It is a [[myrmecophyte]] noted for its [[Mutualism (biology)|mutualistic]] association with a species of [[ant]], ''[[Camponotus schmitzi]]''. As an [[Myrmecotrophy|ant-fed plant]] it lacks many of the features that characterise the carnivorous syndrome in ''Nepenthes'', including [[viscoelasticity|viscoelastic]] and highly acidic pitcher fluid, the waxy zone of the pitcher interior, and possibly even functional [[digestive enzyme]]s.<ref name=Bazile />
{{TOClimit|limit=2}}
{{TOClimit|limit=2}}


Line 62: Line 62:
==Carnivory==
==Carnivory==
[[Image:Serian road side N. bicalcarata 2.jpg|thumb|Upper pitcher with prominent thorns]]
[[Image:Serian road side N. bicalcarata 2.jpg|thumb|Upper pitcher with prominent thorns]]
The two thorns that give ''N.&nbsp;bicalcarata'' its name are unique to this species and bear some of the largest [[nectar]]ies in the plant kingdom.<ref>Merbach, M.A., G. Zizka, B. Fiala, D. Merbach & U. Maschwitz 1999. {{PDFlink|[http://www.gtoe.de/public_html/publications/pdf/5-1/Merbach%20et%20al.%201999,%20Ecotropica%205_45-50.pdf Giant nectaries in the peristome thorns of the pitcher plant ''Nepenthes bicalcarata'' Hooker f. (Nepenthaceae): anatomy and functional aspects.]}} ''Ecotropica'' '''5''': 45–50.</ref><ref>Clarke, C.M. 2001. ''[[A Guide to the Pitcher Plants of Sabah]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref><ref name=C&L>Clarke, C.M. & C.C. Lee 2004. ''[[Pitcher Plants of Sarawak]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref> The purpose of these structures has long been debated among botanists. [[Frederick William Burbidge]] suggested that they might serve to deter [[arboreal]] [[mammal]]s such as [[tarsier]]s, [[loris]]es and [[monkey]]s from stealing the contents of the pitchers. In an article published in 1982, Cliff Dodd speculated on the function of the thorns, but did not believe they play a role in prey capture.<ref name=Dodd>Dodd, C. 1982. {{PDFlink|[http://www.carnivorousplants.org/cpn/articles/CPNv11n3p64_65_73_78.pdf The most dangerous (looking) ''Nepenthes''.]|658&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 674130 bytes -->}} ''[[Carnivorous Plant Newsletter]]'' '''11'''(3): 64–65, 73, 78.</ref> [[Charles Clarke (botanist)|Charles Clarke]] observed that monkeys and tarsiers rip the pitchers open at the sides in order to feed from them, rather than reaching in through the pitcher mouth.<ref name=thorns>Clarke, C.[M.] 1993. {{PDFlink|[http://www.carnivorousplants.org/cpn/articles/CPNv22n1_2p27_28.pdf The possible functions of the thorns of ''Nepenthes bicalcarata'' (Hook.f.) pitchers.]|194&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 199215 bytes -->}} ''[[Carnivorous Plant Newsletter]]'' '''22'''(1–2): 27–28.</ref> However, he found that the mammals attacked the pitchers of ''N.&nbsp;bicalcarata'' less frequently than those of other species, such as ''[[Nepenthes rafflesiana|N.&nbsp;rafflesiana]]''.<ref name=thorns /> Clarke's observations suggest that the spines likely serve to lure insects into a precarious position over the pitcher mouth, where they may lose their footing and fall into the pitcher fluid, eventually drowning.<ref name=thorns />
The two thorns that give ''N.&nbsp;bicalcarata'' its name are unique to this species and bear some of the largest [[nectar]]ies in the plant kingdom.<ref>Merbach, M.A., G. Zizka, B. Fiala, D. Merbach & U. Maschwitz 1999. {{PDFlink|[http://www.gtoe.de/public_html/publications/pdf/5-1/Merbach%20et%20al.%201999,%20Ecotropica%205_45-50.pdf Giant nectaries in the peristome thorns of the pitcher plant ''Nepenthes bicalcarata'' Hooker f. (Nepenthaceae): anatomy and functional aspects.]}} ''Ecotropica'' '''5''': 45–50.</ref><ref>Clarke, C.M. 2001. ''[[A Guide to the Pitcher Plants of Sabah]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref><ref name=C&L>Clarke, C.M. & C.C. Lee 2004. ''[[Pitcher Plants of Sarawak]]''. Natural History Publications (Borneo), Kota Kinabalu.</ref> The purpose of these structures has long been debated among botanists. [[Frederick William Burbidge]] suggested that they might serve to deter [[arboreal]] [[mammal]]s such as [[tarsier]]s, [[loris]]es and [[monkey]]s from stealing the contents of the pitchers. In an article published in 1982, Cliff Dodd speculated on the function of the thorns, but did not believe they play a role in prey capture.<ref name=Dodd>Dodd, C. 1982. {{PDFlink|[http://www.carnivorousplants.org/cpn/articles/CPNv11n3p64_65_73_78.pdf The most dangerous (looking) ''Nepenthes''.]|658&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 674130 bytes -->}} ''[[Carnivorous Plant Newsletter]]'' '''11'''(3): 64–65, 73, 78.</ref> [[Charles Clarke (botanist)|Charles Clarke]] observed that monkeys and tarsiers rip the pitchers open at the sides in order to feed from them, rather than reaching in through the pitcher mouth.<ref name=thorns>Clarke, C.[M.] 1993. {{PDFlink|[http://www.carnivorousplants.org/cpn/articles/CPNv22n1_2p27_28.pdf The possible functions of the thorns of ''Nepenthes bicalcarata'' (Hook.f.) pitchers.]|194&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 199215 bytes -->}} ''[[Carnivorous Plant Newsletter]]'' '''22'''(1–2): 27–28.</ref> However, he found that the mammals attacked the pitchers of ''N.&nbsp;bicalcarata'' less frequently than those of other species, such as ''[[Nepenthes rafflesiana|N.&nbsp;rafflesiana]]''.<ref name=thorns /> Clarke's observations suggest that the spines likely serve to lure insects into a precarious position over the pitcher mouth, where they may lose their footing and fall into the pitcher fluid, eventually drowning.<ref name=thorns /> A similar trapping method is employed by the [[Sumatra]]n endemic ''[[Nepenthes lingulata|N.&nbsp;lingulata]]'', which has a single [[wikt:filiform|filiform]] appendage positioned over the pitcher mouth. However, in that species the appendage is a structure of the lid and not the peristome.<ref name=lingulata>Lee, C.C., Hernawati & P. Akhriadi 2006. [http://www.ingentaconnect.com/content/nhn/blumea/2006/00000051/00000003/art00007 Two new species of ''Nepenthes'' (Nepenthaceae) from North Sumatra]. ''Blumea'' '''51'''(3): 561–568.</ref>


⚫
Together with ''[[Nepenthes ampullaria|N.&nbsp;ampullaria]]'' and ''[[Nepenthes ventricosa|N.&nbsp;ventricosa]]'', ''N.&nbsp;bicalcarata'' is unusual in that the glandular region of the pitcher extends almost to the peristome, such that there is little or no conductive waxy zone.<ref name=Bohn>Bohn, H.F. & W. Federle 2004. {{PDFlink|[http://www.pnas.org/cgi/reprint/101/39/14138.pdf Insect aquaplaning: ''Nepenthes'' pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface.]}} ''[[Proceedings of the National Academy of Sciences]]'' '''101'''(39): 14138–14143.</ref><ref name=Moran2010>Moran, J.A., B.J. Hawkins, B.E. Gowen & S.L. Robbins 2010. Ion fluxes across the pitcher walls of three Bornean ''Nepenthes'' pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. ''Journal of Experimental Botany'' '''61'''(5): 1365–1374. {{DOI|10.1093/jxb/erq004}}</ref><ref>Di Giusto, B., M. Guéroult, N. Rowe & L. Gaume 2009. [http://books.google.co.uk/books?id=RbmuGOwJrSoC&lpg=PR3&pg=PA183#v=onepage&q=&f=false Chapter 7: The Waxy Surface in ''Nepenthes'' Pitcher Plants: Variability, Adaptive Significance and Developmental Evolution]. In: S.N. Gorb (ed.) ''Functional Surfaces in Biology: Adhesion Related Phenomena''. Volume 2. Springer. pp. 183–204.</ref> The waxy zone functions by causing prey to slip and fall into the digestive fluid. A 2004 study found that the peristome of ''N.&nbsp;bicalcarata'' plays a very important role in prey capture. When it is dry, the peristome is highly ineffective in catching insect prey, but when wetted, the capture rate increases more than three-fold.<ref name=Bohn />
A similar trapping method is employed by the [[Sumatra]]n endemic ''[[Nepenthes lingulata|N.&nbsp;lingulata]]'', which has a single [[wikt:filiform|filiform]] appendage positioned over the pitcher mouth. However, in that species the appendage is a structure of the lid and not the peristome.<ref name=lingulata>Lee, C.C., Hernawati & P. Akhriadi 2006. [http://www.ingentaconnect.com/content/nhn/blumea/2006/00000051/00000003/art00007 Two new species of ''Nepenthes'' (Nepenthaceae) from North Sumatra]. ''Blumea'' '''51'''(3): 561–568.</ref>

⚫
Together with ''[[Nepenthes ampullaria|N.&nbsp;ampullaria]]'' and ''[[Nepenthes ventricosa|N.&nbsp;ventricosa]]'', ''N.&nbsp;bicalcarata'' is unusual in that the glandular region of the pitcher extends almost to the peristome, such that there is little or no conductive waxy zone.<ref name=Bohn>Bohn, H.F. & W. Federle 2004. {{PDFlink|[http://www.pnas.org/cgi/reprint/101/39/14138.pdf Insect aquaplaning: ''Nepenthes'' pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface.]}} ''[[Proceedings of the National Academy of Sciences]]'' '''101'''(39): 14138–14143.</ref><ref name=Moran2010>Moran, J.A., B.J. Hawkins, B.E. Gowen & S.L. Robbins 2010. Ion fluxes across the pitcher walls of three Bornean ''Nepenthes'' pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. ''Journal of Experimental Botany'' '''61'''(5): 1365–1374. {{DOI|10.1093/jxb/erq004}}</ref><ref>Di Giusto, B., M. Guéroult, N. Rowe & L. Gaume 2009. [http://books.google.co.uk/books?id=RbmuGOwJrSoC&lpg=PR3&pg=PA183#v=onepage&q=&f=false Chapter 7: The Waxy Surface in ''Nepenthes'' Pitcher Plants: Variability, Adaptive Significance and Developmental Evolution]. In: S.N. Gorb (ed.) ''Functional Surfaces in Biology: Adhesion Related Phenomena''. Volume 2. Springer. pp. 183–204.</ref> The waxy zone functions by causing prey to slip and fall into the digestive fluid. A 2004 study found that the peristome of ''N.&nbsp;bicalcarata'' plays a very important role in prey capture. When it is dry, the peristome is very ineffective in catching insect prey, but when wetted, the capture rate increases more than three-fold.<ref name=Bohn />


A 1999 study of pitcher morphology and spectral reflectance characteristics showed that ''N.&nbsp;bicalcarata'' has no colour contrast maximum between the peristome and pitcher cup in the [[ultraviolet]] waveband, but small maxima of –0.17 at 450&nbsp;nm ([[Violet (color)|violet]]), 0.32 at 548&nbsp;nm ([[green]]), and –0.16 at 668&nbsp;nm ([[red]]).<ref name=spectrum>Moran, J.A., W.E. Booth & J.K. Charles 1999. {{PDFlink|[http://aob.oxfordjournals.org/cgi/reprint/83/5/521.pdf Aspects of Pitcher Morphology and Spectral Characteristics of Six Bornean ''Nepenthes'' Pitcher Plant Species: Implications for Prey Capture.]}} ''Annals of Botany'' '''83''': 521–528.</ref> This means that the peristome is less reflective than the pitcher cup in the violet and red bands, but more reflective in the green band. The contrast maxima in the green and blue regions seem to correspond to insect visual sensitivity maxima, while the others do not.<ref name=spectrum /> Based on their findings, the authors made the "tentative prediction" that the upper pitchers of ''N.&nbsp;bicalcarata'' are less successful at catching anthophilous (flower-visiting) prey than those of sympatric ''N.&nbsp;rafflesiana''.<ref name=spectrum />
A 1999 study of pitcher morphology and spectral reflectance characteristics showed that ''N.&nbsp;bicalcarata'' has no colour contrast maximum between the peristome and pitcher cup in the [[ultraviolet]] waveband, but small maxima of –0.17 at 450&nbsp;nm ([[Violet (color)|violet]]), 0.32 at 548&nbsp;nm ([[green]]), and –0.16 at 668&nbsp;nm ([[red]]).<ref name=spectrum>Moran, J.A., W.E. Booth & J.K. Charles 1999. {{PDFlink|[http://aob.oxfordjournals.org/cgi/reprint/83/5/521.pdf Aspects of Pitcher Morphology and Spectral Characteristics of Six Bornean ''Nepenthes'' Pitcher Plant Species: Implications for Prey Capture.]}} ''Annals of Botany'' '''83''': 521–528.</ref> This means that the peristome is less reflective than the pitcher cup in the violet and red bands, but more reflective in the green band. The contrast maxima in the green and blue regions seem to correspond to insect visual sensitivity maxima, while the others do not.<ref name=spectrum /> Based on their findings, the authors made the "tentative prediction" that the upper pitchers of ''N.&nbsp;bicalcarata'' are less successful at catching anthophilous (flower-visiting) prey than those of sympatric ''N.&nbsp;rafflesiana''.<ref name=spectrum />


==Association with ants and pitcher infauna==
==Association with ants and pitcher infauna==
''Nepenthes bicalcarata'' plays host to an unusual species of [[ant]] that makes its nest in the plant's hollow tendrils.<ref name=Clarke /><ref>Shelford, R. 1916. ''A Naturalist in Borneo''. T. Fisher Unwin, London.</ref><ref>Cresswell, J.E. 2000. Resource input and the community structure of larval infaunas of an eastern tropical pitcher plant ''Nepenthes bicalcarata''. ''Ecological Entomology'' '''25'''(3): 362–366. {{DOI|10.1046/j.1365-2311.2000.00267.x}}</ref><ref>Merbach, M.A., G. Zizka, B. Fiala, U. Maschwitz & W.E. Booth 2000. Carnivory and myrmecophytism—a contradiction? Studies on ''Nepenthes bicalcarata'' Hook.f. and its ants. Tagungsband gtö 2000 13. Jahrestagung der Deutschen Gesellschaft für Tropenökologie 1–3. March 2000 in Würzburg Lehrstuhl für Tierökologie und Tropenbiologie Universität Würzburg. p. 106.</ref> Described as ''[[Camponotus schmitzi]]'' in 1933,<ref>Schuitemaker, J.P. & A. Stärke 1933. Contribution a l'etude de la faune Nepenthicole. Art. III Un noveau ''Camponotus'' de Borneo, habitant les tiges cruises de ''Nepenthes'' récolté par J. P. Schuitemaker et décrit par A. Stärke, den Dolder. ''Overdruk uit het Natuurhistorisch Maandblad'' '''22'''(3): 29–31.</ref> it is a member of the extremely populous and widespread genus of [[carpenter ant]]s.
''Nepenthes bicalcarata'' plays host to an unusual species of [[ant]] that makes its nest in the plant's hollow tendrils.<ref name=Clarke /><ref>Shelford, R. 1916. ''A Naturalist in Borneo''. T. Fisher Unwin, London.</ref><ref>Cresswell, J.E. 2000. Resource input and the community structure of larval infaunas of an eastern tropical pitcher plant ''Nepenthes bicalcarata''. ''Ecological Entomology'' '''25'''(3): 362–366. {{DOI|10.1046/j.1365-2311.2000.00267.x}}</ref><ref>Merbach, M.A., G. Zizka, B. Fiala, U. Maschwitz & W.E. Booth 2000. Carnivory and myrmecophytism—a contradiction? Studies on ''Nepenthes bicalcarata'' Hook.f. and its ants. Tagungsband gtö 2000 13. Jahrestagung der Deutschen Gesellschaft für Tropenökologie 1–3. March 2000 in Würzburg Lehrstuhl für Tierökologie und Tropenbiologie Universität Würzburg. p. 106.</ref> Described as ''[[Camponotus schmitzi]]'' in 1933,<ref>Schuitemaker, J.P. & A. Stärcke 1933. Contribution a l'etude de la faune Nepenthicole. Art. III Un noveau ''Camponotus'' de Borneo, habitant les tiges cruises de ''Nepenthes'' récolté par J. P. Schuitemaker et décrit par A. Stärke, den Dolder. ''Overdruk uit het Natuurhistorisch Maandblad'' '''22'''(3): 29–31.</ref> it is a member of the extremely populous and widespread genus of [[carpenter ant]]s.


[[Image:Bicalcarata-upperpitcher.jpg|thumb|left|Upper pitcher with swollen tendril colonised by ''Camponotus schmitzi''.]]
[[Image:Bicalcarata-upperpitcher.jpg|thumb|left|Upper pitcher with swollen tendril colonised by ''Camponotus schmitzi''.]]


This unique animal–plant interaction was noted by [[Frederick William Burbidge]] as early as 1880.<ref>Burbidge, F.W. 1880. ''The Gardens of the Sun: or, a Naturalist's Journal on the Mountains and in the Forests and Swamps of Borneo and the Sulu Archipelago''. John Murray, London.</ref> In 1904, [[Odoardo Beccari]] suggested that the ants feed on insects found on and around the plant, but may fall prey to it themselves.<ref>Beccari, O. 1904. ''Wanderings in the Great Forests of Borneo''. Archibald and Constable, London.</ref> In 1990, B. Hölldobler and E.O. Wilson proposed that ''N.&nbsp;bicalcarata'' and ''C. schmitzi'' form a [[Mutualism (biology)|mutually beneficial]] association.<ref>Hölldobler, B. & E.O. Wilson 1990. ''The Ants''. Springer-Verlag, Berlin, Germany.</ref> At the time, however, no experimental data existed to support such a hypothesis. A series of observations and experiments carried out in [[Brunei]] by [[Charles Clarke (botanist)|Charles Clarke]] (published in 1992 and 1998),<ref>Clarke, C.M. 1992. The ecology of metazoan communities in ''Nepenthes'' pitcher plants in Borneo, with special reference to the community of ''Nepenthes bicalcarata'' Hook.f. Ph.D. thesis, University of New England, Armidale, New South Wales. 269 pp.</ref><ref>Clarke, C.M. 1998. Initial colonisation and prey capture in ''Nepenthes bicalcarata'' (Nepenthaceae) pitchers in Brunei. ''Sandakania'' '''12''': 27–36.</ref><ref>Clarke, C.M. 1998. The aquatic arthropod community of the pitcher plant, ''Nepenthes bicalcarata'' (Nepenthaceae) in Brunei. ''Sandakania'' '''11''': 55–60.</ref> and by Clarke and Roger Kitching (1993 and 1995),<ref>Clarke, C.M. & R.L. Kitching 1993. The metazoan food webs from six Bornean ''Nepenthes'' species. ''Ecological Entomology'' '''18'''(1): 7–16. {{DOI|10.1111/j.1365-2311.1993.tb01074.x}}</ref><ref>Clarke, C.M. & R.L. Kitching 1995. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. ''Journal of Tropical Ecology'' '''11'''(4): 589–602. {{DOI|10.1017/S0266467400009160}}</ref> strongly support the [[Mutualism (biology)|mutualism]] theory. John Thompson has suggested that ''N.&nbsp;bicalcarata'' may be the only plant species that obtains nutrients through both insect capture and ant-hosting habits.<ref>Thompson, J.H. 1981. Reverse animal-plant interactions: the evolution of insectivorous and ant-fed plants. ''Biological Journal of the Linnean Society'' '''16''': 147–155.</ref>
This unique animal–plant interaction was noted by [[Frederick William Burbidge]] as early as 1880.<ref>Burbidge, F.W. 1880. ''The Gardens of the Sun: or, a Naturalist's Journal on the Mountains and in the Forests and Swamps of Borneo and the Sulu Archipelago''. John Murray, London.</ref> In 1904, [[Odoardo Beccari]] suggested that the ants feed on insects found on and around the plant, but may fall prey to it themselves.<ref>Beccari, O. 1904. ''Wanderings in the Great Forests of Borneo''. Archibald and Constable, London.</ref> In 1990, B. Hölldobler and E.O. Wilson proposed that ''N.&nbsp;bicalcarata'' and ''C. schmitzi'' form a [[Mutualism (biology)|mutually beneficial]] association.<ref>Hölldobler, B. & E.O. Wilson 1990. ''The Ants''. Springer-Verlag, Berlin, Germany.</ref> At the time, however, no experimental data existed to support such a hypothesis. A series of observations and experiments carried out in [[Brunei]] by [[Charles Clarke (botanist)|Charles Clarke]] (published in 1992 and 1998),<ref>Clarke, C.M. 1992. The ecology of metazoan communities in ''Nepenthes'' pitcher plants in Borneo, with special reference to the community of ''Nepenthes bicalcarata'' Hook.f. Ph.D. thesis, University of New England, Armidale, New South Wales. 269 pp.</ref><ref>Clarke, C.M. 1998. Initial colonisation and prey capture in ''Nepenthes bicalcarata'' (Nepenthaceae) pitchers in Brunei. ''Sandakania'' '''12''': 27–36.</ref><ref>Clarke, C.M. 1998. The aquatic arthropod community of the pitcher plant, ''Nepenthes bicalcarata'' (Nepenthaceae) in Brunei. ''Sandakania'' '''11''': 55–60.</ref> and by Clarke and Roger Kitching (1993 and 1995),<ref>Clarke, C.M. & R.L. Kitching 1993. The metazoan food webs from six Bornean ''Nepenthes'' species. ''Ecological Entomology'' '''18'''(1): 7–16. {{DOI|10.1111/j.1365-2311.1993.tb01074.x}}</ref><ref>Clarke, C.M. & R.L. Kitching 1995. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. ''Journal of Tropical Ecology'' '''11'''(4): 589–602. {{DOI|10.1017/S0266467400009160}}</ref> strongly support the [[Mutualism (biology)|mutualism]] theory.

''Nepenthes bicalcarata'' is a [[myrmecotrophy|myrmecotroph]] (ant-fed plant), obtaining nutrients from ''C.&nbsp;schmitzi'' in the form of [[wikt:egesta|egesta]] and, occasionally, ant remains. It has been estimated that this input accounts for 42% of the plant's total foliar [[nitrogen]] (76% in plants with ant occupancy rates above 75%).<ref name=Bazile>Bazile, V., J.A. Moran, G. Le Moguédec, D.J. Marshall & L. Gaume 2012. A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism. ''PLoS ONE'' '''7'''(5): e36179. {{DOI|10.1371/journal.pone.0036179}}</ref><ref>Wrenn, E. 2012. [http://www.dailymail.co.uk/sciencetech/article-2142488/How-carnivorous-insect-eating-plant-colony-ANTS-function-digestive-system.html How a carnivorous, insect-eating plant has a colony of ANTS to function as a digestive system]. ''Daily Mail'', May 10, 2012.</ref> ''Camponotus schmitzi'' has also been observed to attack newly caught insects and therefore prevent prey escape.<ref name=Bonhomme>Bonhomme, V., I. Gounand, C. Alaux, E. Jousselin, D. Barthélémy & L. Gaume 2011. {{PDFlink|[http://isabellegounand.files.wordpress.com/2010/12/bonhomme-et-al_2011_jte.pdf The plant-ant ''Camponotus schmitzi'' helps its carnivorous host-plant ''Nepenthes bicalcarata'' to catch its prey.]}} ''Journal of Tropical Ecology'' '''27''': 15–24. {{DOI|10.1017/S0266467410000532}}</ref><ref>{{fr icon}} Gaume, L. N.d. [http://umramap.cirad.fr/amap3/cm/index.php?page=piege-mutualiste-2 Piège mutualiste]. [video] UMR AMAP.</ref> At other times, the ants are very passive, remaining hidden under the inner peristome fold, presumably so as not to dissuade visitation by potential prey species.<ref name=Bonhomme /> This behaviour is in stark contrast to other [[myrmecophyte|myrmecophytic]] ants, which are typically highly territorial.<ref name=Bonhomme /> John Thompson has suggested that ''N.&nbsp;bicalcarata'' may be the only plant species that obtains nutrients through both insect capture and ant-hosting habits.<ref>Thompson, J.H. 1981. Reverse animal-plant interactions: the evolution of insectivorous and ant-fed plants. ''Biological Journal of the Linnean Society'' '''16''': 147–155.</ref>

⚫
''Camponotus schmitzi'' is able to swim in the pitcher fluid using tripod-like leg coordination similar to that of terrestrial locomotion.<ref>Bohn, H.F., D.G. Thornham & W. Federle 2012. Ants swimming in pitcher plants: kinematics of aquatic and terrestrial locomotion in ''Camponotus schmitzi''. ''Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology'', published online on April 17, 2012. {{DOI|10.1007/s00359-012-0723-4}}</ref><ref>de Lange, C. 2012. [http://www.newscientist.com/article/dn21747-zoologger-the-ant-that-dives-into-digestive-juices.html Zoologger: The ant that dives into digestive juices]. ''New Scientist'', April 26, 2012.</ref> The ants feed by descending into the pitcher fluid and retrieving the prey within, apparently targetting only larger items. Hauling food from the pitcher fluid to the peristome—a distance of no more than 5&nbsp;cm—may take up to 12 hours.<ref name=Clarke /> In this way the contents of ''N.&nbsp;bicalcarata'' pitchers is controlled such that organic matter does not accumulate to the point of [[putrefaction]], which could lead to the demise of [[nepenthes infauna|pitcher infauna]] (which also appear to benefit the plant) and sometimes the pitcher itself.<ref name=Clarke /><ref>Hansen, E. 2001. [http://discovermagazine.com/2001/oct/featplants Where rocks sing, ants swim, and plants eat animals: finding members of the ''Nepenthes'' carnivorous plant family in Borneo]. ''Discover'' '''22'''(10): 60–68.</ref>


[[File:Nepenthes bicalcarata and Camponotus schmitzi.png|thumb|''[[Camponotus schmitzi]]'' and ''[[Alcidodes]]'' sp. in association with ''N.&nbsp;bicalcarata'']]
⚫
''Camponotus schmitzi'' is able to swim in pitcher fluid using tripod-like leg coordination similar to that of terrestrial locomotion.<ref>Bohn, H.F., D.G. Thornham & W. Federle 2012. Ants swimming in pitcher plants: kinematics of aquatic and terrestrial locomotion in ''Camponotus schmitzi''. ''Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology'', published online on April 17, 2012. {{DOI|10.1007/s00359-012-0723-4}}</ref><ref>de Lange, C. 2012. [http://www.newscientist.com/article/dn21747-zoologger-the-ant-that-dives-into-digestive-juices.html Zoologger: The ant that dives into digestive juices]. ''New Scientist'', April 26, 2012.</ref> The ants feed by descending into the pitcher fluid and retrieving [[arthropod]]s caught by the plant. They seem to ignore smaller insects and only target larger prey items. Hauling food from the pitcher fluid to the peristome—a distance of no more than 5&nbsp;cm—may take up to 12 hours.<ref name=Clarke /> In this way the contents of ''N.&nbsp;bicalcarata'' pitchers is controlled such that organic matter does not accumulate to the point of [[putrefaction]], which could lead to the demise of [[nepenthes infauna|pitcher infauna]] (which also appear to benefit the plant) and sometimes the pitcher itself.<ref name=Clarke /><ref>Hansen, E. 2001. [http://discovermagazine.com/2001/oct/featplants Where rocks sing, ants swim, and plants eat animals: finding members of the ''Nepenthes'' carnivorous plant family in Borneo]. ''Discover'' '''22'''(10): 60–68.</ref> The ants have also been observed to attack newly caught insects and therefore prevent prey escape.<ref name=Bonhomme>Bonhomme, V., I. Gounand, C. Alaux, E. Jousselin, D. Barthélémy & L. Gaume 2011. {{PDFlink|[http://isabellegounand.files.wordpress.com/2010/12/bonhomme-et-al_2011_jte.pdf The plant-ant ''Camponotus schmitzi'' helps its carnivorous host-plant ''Nepenthes bicalcarata'' to catch its prey.]}} ''Journal of Tropical Ecology'' '''27''': 15–24. {{DOI|10.1017/S0266467410000532}}</ref> At other times, the ants are very passive, remaining hidden under the inner peristome fold, presumably so as not to dissuade visitation by potential prey species.<ref name=Bonhomme /> This behaviour is in stark contrast to other [[myrmecophyte|myrmecophytic]] ants, which are typically highly territorial.<ref name=Bonhomme />


The ants have been observed to clean the peristome of fungal [[hyphae]] and other contaminants, thereby maintaining high trapping efficiency over the pitcher's lifespan.<ref>Thornham, D.G., J.M. Smith, T.U. Grafe & W. Federle 2012. Setting the trap: cleaning behaviour of ''Camponotus schmitzi'' ants increases long-term capture efficiency of their pitcher plant host, ''Nepenthes bicalcarata''. ''Functional Ecology'' '''26'''(1): 11–19. {{DOI|10.1111/j.1365-2435.2011.01937.x}}</ref> Research conducted by Dennis and Marlis Merbach has shown that ''C. schmitzi'' is also beneficial to ''N.&nbsp;bicalcarata'' in that it protects it from pitcher-destroying [[weevil]]s of the genus ''[[Alcidodes]]''.<ref>Merbach, M.A., G. Zizka, B. Fiala, D.J. Merbach, W.E. Booth & U. Maschwitz 2007. {{PDFlink|[http://www.gtoe.de/PDF/Ecotropica_2007_01/Merbach%20et%20al%202007,%20Ecotropica%2013-1.pdf Why a carnivorous plant cooperates with an ant – selective defense against pitcher-destroying weevils in the myrmecophytic pitcher plant ''Nepenthes bicalcarata'' Hook.f..]}} ''Ecotropica'' '''13''': 45–56.</ref><ref>Merbach, M.A. & D.J. Merbach 2002. {{PDFlink|[http://www.muk.uni-frankfurt.de/Publikationen/FFFM/dok/2002/2002-3/Fleischfressende-Kannenpflanze_74-77.pdf Auf der Suche nach Nahrung in die Todesfalle.]|116&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 119690 bytes -->}} ''Forschung Frankfurt'' 2002(3): 74–77.</ref> In order to create a favourable environment for its pitcher inhabitants, it appears that ''N.&nbsp;bicalcarata'' actively maintains the [[pH]] of the pitcher fluid at a less acidic level than that found in most other ''Nepenthes'' species.<ref name=Moran2010 /><ref name=Bonhomme /> This might explain the occasional presence of [[tree frog]] eggs, which are sensitive to strongly acidic conditions, in the pitchers of this species.<ref name=Moran2010 />
The ants have been observed to clean the peristome of fungal [[hyphae]] and other contaminants, thereby maintaining high trapping efficiency over the pitcher's lifespan.<ref>Thornham, D.G., J.M. Smith, T.U. Grafe & W. Federle 2012. Setting the trap: cleaning behaviour of ''Camponotus schmitzi'' ants increases long-term capture efficiency of their pitcher plant host, ''Nepenthes bicalcarata''. ''Functional Ecology'' '''26'''(1): 11–19. {{DOI|10.1111/j.1365-2435.2011.01937.x}}</ref> Research conducted by Dennis and Marlis Merbach has shown that ''C.&nbsp;schmitzi'' also benefits ''N.&nbsp;bicalcarata'' by protecting it from pitcher-destroying [[weevil]]s of the genus ''[[Alcidodes]]''.<ref>Merbach, M.A., G. Zizka, B. Fiala, D.J. Merbach, W.E. Booth & U. Maschwitz 2007. {{PDFlink|[http://www.gtoe.de/PDF/Ecotropica_2007_01/Merbach%20et%20al%202007,%20Ecotropica%2013-1.pdf Why a carnivorous plant cooperates with an ant – selective defense against pitcher-destroying weevils in the myrmecophytic pitcher plant ''Nepenthes bicalcarata'' Hook.f..]}} ''Ecotropica'' '''13''': 45–56.</ref><ref>Merbach, M.A. & D.J. Merbach 2002. {{PDFlink|[http://www.muk.uni-frankfurt.de/Publikationen/FFFM/dok/2002/2002-3/Fleischfressende-Kannenpflanze_74-77.pdf Auf der Suche nach Nahrung in die Todesfalle.]|116&nbsp;[[Kibibyte|KiB]]<!-- application/pdf, 119690 bytes -->}} ''Forschung Frankfurt'' 2002(3): 74–77.</ref> In order to create a favourable environment for its pitcher inhabitants, it appears that ''N.&nbsp;bicalcarata'' actively maintains the [[pH]] of its pitcher fluid at a less acidic level than that found in most other ''Nepenthes'' species<ref name=Moran2010 /><ref name=Bonhomme /> (this might explain the occasional presence of [[tree frog]] eggs in its pitchers).<ref name=Moran2010 /> In doing so, however, the plant reduces its ability to digest and assimilate nutrients from captured prey. The pitcher fluid of ''N.&nbsp;bicalcarata'' is also less [[viscoelasticity|viscoelastic]] than that of most ''Nepenthes'' species, and appears to lack functional [[digestive enzymes]].<ref name=Bazile /> ''Nepenthes bicalcarata'' is therefore highly reliant on its ant symbiont. Indeed, plants not inhabited by ''C.&nbsp;schmitzi'' do not appear to benefit significantly from carnivory, with any gains from prey digestion being offset by the high costs of pitcher construction.<ref name=Bazile /> Conversely, ant-inhabited plants have more leaves and a greater total leaf area, and ant presence is associated with lower pitcher abortion rates and more voluminous pitchers (and consequently greater prey [[biomass]]).<ref name=Bazile /><ref>Choi, C. 2012. [http://www.livescience.com/20192-carnivorous-plants-employ-bodyguard-ants.html Carnivorous plants employ bodyguard ants]. ''LiveScience'', May 9, 2012.</ref><ref>Steadman, I. 2012. [http://www.wired.co.uk/news/archive/2012-05/10/carnivorous-plants-eat-ant-poop Carnivorous plants offer ants shelter in return for faeces and protection]. ''Wired'', May 10, 2012.</ref>


The ants seem to favour upper pitchers and rarely colonise lower pitchers.<ref>Clarke, C.M. 1997. The effects of pitcher dimorphism on the metazoan community of the carnivorous pitcher plant ''Nepenthes bicalcarata'' Hook.f.. ''Malayan Nature Journal'' '''50''': 149–157.</ref> This is likely due to the fact that terrestrial traps are periodically submerged in water during heavy rains. Flooding of the ants' nest chamber could result in the death of the developing eggs, [[larva]]e, and [[pupa]]e.<ref name=C&L /> ''Camponotus schmitzi'' nests solely in the tendrils of ''N.&nbsp;bicalcarata'' and rarely ventures onto other plants. The species is completely dependent on ''N.&nbsp;bicalcarata'' for food and [[wikt:domicile|domicile]].<ref name=Clarke /> ''Nepenthes bicalcarata'', on the other hand, is able to survive and reproduce without the presence of the ants; it is a [[Mutualism (biology)|facultative mutualist]]. This being the case, there appear to be few mature plants over 2 metres in height not colonised by ''C. schmitzi''.<ref name=Clarke />
''Camponotus schmitzi'' nests solely in the tendrils of ''N.&nbsp;bicalcarata'' and rarely ventures onto other plants. The species is completely dependent on ''N.&nbsp;bicalcarata'' for food and [[wikt:domicile|domicile]].<ref name=Clarke /> ''Nepenthes bicalcarata'', on the other hand, is able to survive and reproduce without the presence of the ants; it is a [[Mutualism (biology)|facultative mutualist]]. This being the case, there appear to be few mature plants over 2 metres in height not colonised by ''C. schmitzi''.<ref name=Clarke /> The ants seem to favour upper pitchers and rarely colonise lower pitchers.<ref>Clarke, C.M. 1997. The effects of pitcher dimorphism on the metazoan community of the carnivorous pitcher plant ''Nepenthes bicalcarata'' Hook.f.. ''Malayan Nature Journal'' '''50''': 149–157.</ref> This is likely due to the fact that terrestrial traps are periodically submerged in water during heavy rains. Flooding of the ants' nest chamber could result in the death of the developing eggs, [[larva]]e, and [[pupa]]e.<ref name=C&L />


A species of [[mite]], ''[[Naiadacarus nepenthicola]]'', appears to be restricted to the pitchers of ''N.&nbsp;bicalcarata''. It is thought to feed on decomposing leaves and insects that are caught in the pitchers. [[Deutonymph]]s of this mite are dispersed through [[phoresy]] on ''C. schmitzi''.<ref>Fashing, N.J. & T.H. Chua 2002. {{PDFlink|[http://njfash.people.wm.edu/naiadacarus%20.pdf Systematics and ecology of ''Naiadacarus nepenthicola'', a new species of Acaridae (Acari : Astigmata) inhabiting the pitchers of ''Nepenthes bicalcarata'' Hook. f. in Brunei Darussalam.]|2.12&nbsp;[[Mebibyte|MiB]]<!-- application/pdf, 2228189 bytes -->}} ''International Journal of Acarology'' '''28'''(2): 157–167.</ref>
A species of [[mite]], ''[[Naiadacarus nepenthicola]]'', appears to be restricted to the pitchers of ''N.&nbsp;bicalcarata''. It is thought to feed on decomposing leaves and insects that are caught in the pitchers. [[Deutonymph]]s of this mite are dispersed through [[phoresy]] on ''C. schmitzi''.<ref>Fashing, N.J. & T.H. Chua 2002. {{PDFlink|[http://njfash.people.wm.edu/naiadacarus%20.pdf Systematics and ecology of ''Naiadacarus nepenthicola'', a new species of Acaridae (Acari : Astigmata) inhabiting the pitchers of ''Nepenthes bicalcarata'' Hook. f. in Brunei Darussalam.]|2.12&nbsp;[[Mebibyte|MiB]]<!-- application/pdf, 2228189 bytes -->}} ''International Journal of Acarology'' '''28'''(2): 157–167.</ref>
Line 126: Line 128:
===(''N.&nbsp;bicalcarata'' &times; ''N.&nbsp;rafflesiana'') &times; ''N.&nbsp;mirabilis'' var. ''echinostoma''===
===(''N.&nbsp;bicalcarata'' &times; ''N.&nbsp;rafflesiana'') &times; ''N.&nbsp;mirabilis'' var. ''echinostoma''===


[[Charles Clarke (botanist)|Charles Clarke]] reported a single plant displaying characters intermediate in form between ''N.&nbsp;bicalcarata'', ''N.&nbsp;rafflesiana'' and ''N.&nbsp;mirabilis'' var. ''echinostoma'' growing among populations of these species. It is likely a complex hybrid, although this cannot be proven without the use of [[genetic testing]].<ref name=Clarke />
[[Charles Clarke (botanist)|Charles Clarke]] reported a single plant displaying characters intermediate between those of ''N.&nbsp;bicalcarata'', ''N.&nbsp;rafflesiana'' and ''N.&nbsp;mirabilis'' var. ''echinostoma'', and growing among populations of these species. It is likely a complex hybrid, although this cannot be proven without the use of [[DNA sequencing|molecular techniques]].<ref name=Clarke />


==Cultivation and cultivars==
==Cultivation and cultivars==
Line 152: Line 154:
* Fashing, N.J. 2010. {{PDFlink|[http://njfash.people.wm.edu/Trends%20in%20Acarology%202009.pdf Two novel adaptations for dispersal in the mite family Histiostomatidae (Astigmata).]}} In: M.W. Sabelis & J. Bruin (eds.) ''[http://books.google.co.uk/books?id=BBGkhCHzyfkC Trends in Acarology: Proceedings of the 12th International Congress]''. Springer Science, Dordrecht. pp.&nbsp;81–84. {{DOI|10.1007/978-90-481-9837-5}}
* Fashing, N.J. 2010. {{PDFlink|[http://njfash.people.wm.edu/Trends%20in%20Acarology%202009.pdf Two novel adaptations for dispersal in the mite family Histiostomatidae (Astigmata).]}} In: M.W. Sabelis & J. Bruin (eds.) ''[http://books.google.co.uk/books?id=BBGkhCHzyfkC Trends in Acarology: Proceedings of the 12th International Congress]''. Springer Science, Dordrecht. pp.&nbsp;81–84. {{DOI|10.1007/978-90-481-9837-5}}
* Fretwell, S. 2010. Twelve days in Borneo – a dream expedition: part 4. ''[[Victorian Carnivorous Plant Society Journal]]'' '''98''': 6–13.
* Fretwell, S. 2010. Twelve days in Borneo – a dream expedition: part 4. ''[[Victorian Carnivorous Plant Society Journal]]'' '''98''': 6–13.
* {{fr icon}} Gaume, L. N.d. [http://umramap.cirad.fr/amap3/cm/index.php?page=piege-mutualiste-2 Piège mutualiste]. [video] UMR AMAP.
* Kitching, R.L. 2000. [http://books.google.co.uk/books?id=B4F2XYMmRG0C ''Food Webs and Container Habitats: The natural history and ecology of phytotelmata'']. Cambridge University Press, Cambridge.
* Kitching, R.L. 2000. [http://books.google.co.uk/books?id=B4F2XYMmRG0C ''Food Webs and Container Habitats: The natural history and ecology of phytotelmata'']. Cambridge University Press, Cambridge.
* {{cs icon}} Kubeš, V. 2003. [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/07.png "Panel story" o pěstování láčkovky ''Nepenthes bicalcarata'']. ''[[Trifid (journal)|Trifid]]'' '''2003'''(2): 7–10. ([http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/08.png page 2], [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/09.png page 3], [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/10.png page 4])
* {{cs icon}} Kubeš, V. 2003. [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/07.png "Panel story" o pěstování láčkovky ''Nepenthes bicalcarata'']. ''[[Trifid (journal)|Trifid]]'' '''2003'''(2): 7–10. ([http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/08.png page 2], [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/09.png page 3], [http://www.darwiniana.cz/sklad/sklad/Trifid/skeny/600DPI/T2003_2/10.png page 4])

Revision as of 16:00, 12 May 2012

Nepenthes bicalcarata
Intermediate pitcher of N. bicalcarata
Scientific classification
Kingdom:
Plantae
(unranked):
Angiosperms
(unranked):
Eudicots
(unranked):
Core eudicots
Order:
Caryophyllales
Family:
Nepenthaceae
Genus:
Nepenthes
Species:
N. bicalcarata
Binomial name
Nepenthes bicalcarata
Hook.f. (1873)[1]
Synonyms

Nepenthes bicalcarata (/[invalid input: 'icon']n[invalid input: 'ɨ']ˈpɛnθiːz baɪˌkælkəˈrɑːtə/ or /bɪˌkælkəˈreɪtə/; Latin: bi "two", calcaratus "spur"), also known as the Fanged Pitcher-Plant,[3] is a tropical pitcher plant endemic to northwestern Borneo. It is a myrmecophyte noted for its mutualistic association with a species of ant, Camponotus schmitzi. As an ant-fed plant it lacks many of the features that characterise the carnivorous syndrome in Nepenthes, including viscoelastic and highly acidic pitcher fluid, the waxy zone of the pitcher interior, and possibly even functional digestive enzymes.[4]

Botanical history

Illustration of N. bicalcarata from Macfarlane's 1908 monograph

Nepenthes bicalcarata was formally described by Joseph Dalton Hooker in his 1873 monograph, "Nepenthaceae", based on specimens collected by Hugh Low and Odoardo Beccari near Lawas River in Borneo.[1] The type specimen, Low s.n., is deposited at the Royal Botanic Gardens, Kew.[5] Seven years later, Spencer Le Marchant Moore described Nepenthes dyak, based on a specimen collected by Johannes Elias Teijsmann, Teijsmann 10962, from Kapuas River near Sintang in western Borneo.[2][6] This specimen is also held at the Royal Botanic Gardens, Kew[5] and a duplicate is deposited at the National Herbarium of the Netherlands in Leiden.[7] Nepenthes dyak was later mentioned several more times in the botanical literature,[8][9] but is now considered conspecific with N. bicalcarta.[10]

Nepenthes bicalcarata was introduced to Europe in 1879 by British explorer Frederick William Burbidge, who collected plants for the famous Veitch Nursery. These were cultivated to larger size and distributed in 1881.[3]

During this time, interest in Nepenthes had reached its peak. A note in The Gardeners' Chronicle of 1881 mentions the Veitch Nursery's N. bicalcarata as follows:[11]

"Then there is N. bicalcarata, a most robust habited kind with sturdy foliage and bag-like pitchers provided with a vicious-looking rat-trap-like apparatus in its lid which renders it very distinct from its neighbours."

Several years after its introduction, N. bicalcarata was still very much a horticultural rarity. In Veitch's catalogue for 1889, N. bicalcarata was priced at £3.3s per plant, while the famous giant-pitchered N. northiana and N. rajah were selling for £2.2s.[3]

Description

Nepenthes bicalcarata plants are the largest in the genus, climbing up to 20 m into the forest canopy. The cylindrical stem is thicker than that of any other Nepenthes species, measuring up to 3.5 cm in diameter. Internodes are up to 40 cm long.[10][12]

Climbing plant with upper pitchers

The leaves of N. bicalcarata are petiolate and coriaceous in texture. The lamina is obovate-lanceolate in form and also reaches huge dimensions, growing to 80 cm in length and 12 cm in width.[13] It is slightly decurrent on the stem, forming two narrow wings. The lamina has indistinct longitudinal veins and numerous pennate veins. Tendrils may be up to 60 cm long and 8 mm wide. They are hollow and swollen near the pitcher.[10]

Lower pitchers

Although most parts of the plant are very large, the pitchers themselves do not rival those of species such as N. rajah. Nevertheless, they may have a volume of over one litre and grow up to 25 cm high and 16 cm wide. A pair of prominent fringed wings (≤15 mm wide) run down the front of lower pitchers. These are usually reduced to ribs in aerial pitchers. The peristome (≤20 mm wide) is characteristically flattened and curved inwards. It bears small but distinct teeth. The two sharp spines for which the species is famous are present on the underside of the pitcher lid, and may be 3 cm long. They are derived from the uppermost 10–12 peristome ribs.[14] The pitcher lid or operculum is reniform to cordate and has no appendages. An unbranched spur (≤15 mm long) is inserted at the base of the lid.[10]

Nepenthes bicalcarata has a paniculate inflorescence. The peduncle may be up to 40 cm long and the rachis can reach 100 cm in length. Female inflorescences are usually shorter.[15] Branches on the flower stem are up to 40 mm long and bear up to 15 flowers. Sepals are either obovate or lanceolate and up to 4 mm long.[10] A study of 120 pollen samples taken from a herbarium specimen (Fosberg 43860, altitude not recorded) found the mean pollen diameter to be 28.9 μm (SE = 0.4; CV = 7.5%).[16]

Mature plants are virtually glabrous. Caducous hairs are present on the youngest parts of the plant and on the inflorescences.

Nepenthes bicalcarata varies little across its range. Consequently, no infraspecific taxa have been described.[10]

Ecology and conservation status

Natural habitat of N. bicalcarata

Nepenthes bicalcarata is endemic to Borneo. It is most common in the peat swamp forests of the western coast of the island, which stretch across Sarawak, Sabah, Kalimantan, and Brunei. There it often grows in the shade of the ubiquitous dipterocarp Shorea albida.[3] Nepenthes bicalcarata also occurs in kerangas forest and has even been recorded from white sand heath forests in Sarawak and East Kalimantan.[3] The species is often sympatric with N. ampullaria in these habitats.[10]

Specimens growing in undisturbed peat swamp forest, where sunlight is greatly diffused and high humidity prevails, reach the largest dimensions.[10] Nepenthes bicalcarata has a shallow root system that only penetrates the top layer of peat and leaf litter, to a depth of about 25 cm. Below this, high concentrations of tannins and alkaloids render the substrate toxic.[3]

Nepenthes bicalcarata is generally found below 300 m in altitude, although Johannes Gottfried Hallier reported a single collection in 1894 from between 700 and 950 m above sea level.[17]

The conservation status of N. bicalcarata is listed as Vulnerable on the 2006 IUCN Red List of Threatened Species based on an assessment carried out in 2000.[18] In 1997, Charles Clarke informally classified the species as Near Threatened based on the IUCN criteria.[10] This agrees with the conservation status assigned to N. bicalcarata by the World Conservation Monitoring Centre.[19]

Carnivory

Upper pitcher with prominent thorns

The two thorns that give N. bicalcarata its name are unique to this species and bear some of the largest nectaries in the plant kingdom.[20][21][22] The purpose of these structures has long been debated among botanists. Frederick William Burbidge suggested that they might serve to deter arboreal mammals such as tarsiers, lorises and monkeys from stealing the contents of the pitchers. In an article published in 1982, Cliff Dodd speculated on the function of the thorns, but did not believe they play a role in prey capture.[23] Charles Clarke observed that monkeys and tarsiers rip the pitchers open at the sides in order to feed from them, rather than reaching in through the pitcher mouth.[24] However, he found that the mammals attacked the pitchers of N. bicalcarata less frequently than those of other species, such as N. rafflesiana.[24] Clarke's observations suggest that the spines likely serve to lure insects into a precarious position over the pitcher mouth, where they may lose their footing and fall into the pitcher fluid, eventually drowning.[24] A similar trapping method is employed by the Sumatran endemic N. lingulata, which has a single filiform appendage positioned over the pitcher mouth. However, in that species the appendage is a structure of the lid and not the peristome.[25]

Together with N. ampullaria and N. ventricosa, N. bicalcarata is unusual in that the glandular region of the pitcher extends almost to the peristome, such that there is little or no conductive waxy zone.[26][27][28] The waxy zone functions by causing prey to slip and fall into the digestive fluid. A 2004 study found that the peristome of N. bicalcarata plays a very important role in prey capture. When it is dry, the peristome is highly ineffective in catching insect prey, but when wetted, the capture rate increases more than three-fold.[26]

A 1999 study of pitcher morphology and spectral reflectance characteristics showed that N. bicalcarata has no colour contrast maximum between the peristome and pitcher cup in the ultraviolet waveband, but small maxima of –0.17 at 450 nm (violet), 0.32 at 548 nm (green), and –0.16 at 668 nm (red).[29] This means that the peristome is less reflective than the pitcher cup in the violet and red bands, but more reflective in the green band. The contrast maxima in the green and blue regions seem to correspond to insect visual sensitivity maxima, while the others do not.[29] Based on their findings, the authors made the "tentative prediction" that the upper pitchers of N. bicalcarata are less successful at catching anthophilous (flower-visiting) prey than those of sympatric N. rafflesiana.[29]

Association with ants and pitcher infauna

Nepenthes bicalcarata plays host to an unusual species of ant that makes its nest in the plant's hollow tendrils.[10][30][31][32] Described as Camponotus schmitzi in 1933,[33] it is a member of the extremely populous and widespread genus of carpenter ants.

Upper pitcher with swollen tendril colonised by Camponotus schmitzi.

This unique animal–plant interaction was noted by Frederick William Burbidge as early as 1880.[34] In 1904, Odoardo Beccari suggested that the ants feed on insects found on and around the plant, but may fall prey to it themselves.[35] In 1990, B. Hölldobler and E.O. Wilson proposed that N. bicalcarata and C. schmitzi form a mutually beneficial association.[36] At the time, however, no experimental data existed to support such a hypothesis. A series of observations and experiments carried out in Brunei by Charles Clarke (published in 1992 and 1998),[37][38][39] and by Clarke and Roger Kitching (1993 and 1995),[40][41] strongly support the mutualism theory.

Nepenthes bicalcarata is a myrmecotroph (ant-fed plant), obtaining nutrients from C. schmitzi in the form of egesta and, occasionally, ant remains. It has been estimated that this input accounts for 42% of the plant's total foliar nitrogen (76% in plants with ant occupancy rates above 75%).[4][42] Camponotus schmitzi has also been observed to attack newly caught insects and therefore prevent prey escape.[43][44] At other times, the ants are very passive, remaining hidden under the inner peristome fold, presumably so as not to dissuade visitation by potential prey species.[43] This behaviour is in stark contrast to other myrmecophytic ants, which are typically highly territorial.[43] John Thompson has suggested that N. bicalcarata may be the only plant species that obtains nutrients through both insect capture and ant-hosting habits.[45]

Camponotus schmitzi is able to swim in the pitcher fluid using tripod-like leg coordination similar to that of terrestrial locomotion.[46][47] The ants feed by descending into the pitcher fluid and retrieving the prey within, apparently targetting only larger items. Hauling food from the pitcher fluid to the peristome—a distance of no more than 5 cm—may take up to 12 hours.[10] In this way the contents of N. bicalcarata pitchers is controlled such that organic matter does not accumulate to the point of putrefaction, which could lead to the demise of pitcher infauna (which also appear to benefit the plant) and sometimes the pitcher itself.[10][48]

Camponotus schmitzi and Alcidodes sp. in association with N. bicalcarata

The ants have been observed to clean the peristome of fungal hyphae and other contaminants, thereby maintaining high trapping efficiency over the pitcher's lifespan.[49] Research conducted by Dennis and Marlis Merbach has shown that C. schmitzi also benefits N. bicalcarata by protecting it from pitcher-destroying weevils of the genus Alcidodes.[50][51] In order to create a favourable environment for its pitcher inhabitants, it appears that N. bicalcarata actively maintains the pH of its pitcher fluid at a less acidic level than that found in most other Nepenthes species[27][43] (this might explain the occasional presence of tree frog eggs in its pitchers).[27] In doing so, however, the plant reduces its ability to digest and assimilate nutrients from captured prey. The pitcher fluid of N. bicalcarata is also less viscoelastic than that of most Nepenthes species, and appears to lack functional digestive enzymes.[4] Nepenthes bicalcarata is therefore highly reliant on its ant symbiont. Indeed, plants not inhabited by C. schmitzi do not appear to benefit significantly from carnivory, with any gains from prey digestion being offset by the high costs of pitcher construction.[4] Conversely, ant-inhabited plants have more leaves and a greater total leaf area, and ant presence is associated with lower pitcher abortion rates and more voluminous pitchers (and consequently greater prey biomass).[4][52][53]

Camponotus schmitzi nests solely in the tendrils of N. bicalcarata and rarely ventures onto other plants. The species is completely dependent on N. bicalcarata for food and domicile.[10] Nepenthes bicalcarata, on the other hand, is able to survive and reproduce without the presence of the ants; it is a facultative mutualist. This being the case, there appear to be few mature plants over 2 metres in height not colonised by C. schmitzi.[10] The ants seem to favour upper pitchers and rarely colonise lower pitchers.[54] This is likely due to the fact that terrestrial traps are periodically submerged in water during heavy rains. Flooding of the ants' nest chamber could result in the death of the developing eggs, larvae, and pupae.[22]

A species of mite, Naiadacarus nepenthicola, appears to be restricted to the pitchers of N. bicalcarata. It is thought to feed on decomposing leaves and insects that are caught in the pitchers. Deutonymphs of this mite are dispersed through phoresy on C. schmitzi.[55]

Natural hybrids

The following natural hybrids involving N. bicalcarata have been recorded.

None of these hybrids are known to be colonised by C. schmitzi as is the parent species N. bicalcarata.[10]

N. ampullaria × N. bicalcarata

Lower pitcher of N. ampullaria × N. bicalcarata (cultivated)

Since N. ampullaria and N. bicalcarata are often sympatric in the wild, it is not surprising that they occasionally hybridise. Several examples of this natural hybrid are known from Brunei, where it grows in peat swamp forest and heath forest.[10] It was first recorded by Mitsuru Hotta in 1966.[57]

Pitchers bear the characteristic thorns of N. bicalcarata, although they are greatly reduced in size. The mouth is round and the lid is ovate-cordate in form. This hybrid resembles N. × hookeriana to a certain extent, but differs in having spines on the underside of the lid and more globose upper pitchers with a smaller lid.[10]

Aerial pitchers of N. ampullaria × N. bicalcarata are usually dominated by characteristics of N. ampullaria. They are often very small and unable to function in a normal manner.[10]

(N. ampullaria × N. gracilis) × N. bicalcarata

This rare complex hybrid was discovered in the lowland forests of Brunei. It produces small speckled pitchers with reduced thorns under the lid. The plant is intermediate in appearance between N. × trichocarpa and N. bicalcarata.

N. bicalcarata × N. gracilis

Main article: Nepenthes × cantleyi
Lower pitcher of Nepenthes × cantleyi

This hybrid has been named N. × cantleyi after Rob Cantley. The morphology of the pitchers closely resembles N. bicalacarata, although the peristome is more similar to that of N. gracilis. The characteristic spines of N. bicalcarata are greatly reduced and are only present as small bumps. This hybrid has the growth habit of N. gracilis, with the stem scrambling along the ground. It grows in open, sandy areas. The pitcher fluid is notably acidic like that of N. gracilis, with pH values as low as 1.82 being recorded.[10]

N. bicalcarata × N. mirabilis var. echinostoma

This natural hybrid is rare and is only known from Brunei, where it involves N. mirabilis var. echinostoma. It closely resembles N. bicalcarata, although it differs from that species in having reduced thorns and a wider peristome. Unlike N. bicalcarata, this hybrid inhabits open areas with sandy substrates.[10]

N. bicalcarata × N. rafflesiana

This relatively rare natural hybrid is sometimes found growing among populations of N. bicalcarata and N. rafflesiana. It is intermediate in form between its parent species.

(N. bicalcarata × N. rafflesiana) × N. mirabilis var. echinostoma

Charles Clarke reported a single plant displaying characters intermediate between those of N. bicalcarata, N. rafflesiana and N. mirabilis var. echinostoma, and growing among populations of these species. It is likely a complex hybrid, although this cannot be proven without the use of molecular techniques.[10]

Cultivation and cultivars

Lower pitcher of a plant cultivated in Kuching, Sarawak.

Nepenthes bicalcarata may be cultivated in a similar manner to other members of the genus, though it requires relatively hot and humid conditions.[23][58] It needs large pots to do well, and temporary halts in growth are often due to becoming root-bound. Re-potting to a larger pot will often result in a rapid size increase. Under satisfactory conditions, this plant will grow quite fast for a Nepenthes, reaching a large size relatively rapidly.

Despite naturally occurring in peat swamp forests, N. bicalcarata has been successfully grown in a completely inorganic substrate consisting of one part each of Seramis clay perls, lava gravel, and Lecaton expanded clay perls.[59]

Nepenthes bicalcarata has been artificially crossed with N. hirsuta. A particularly robust-pitchered cultivar of this hybrid was named Nepenthes 'Hortulanus Otten', in honour of Karel Otten, former curator of the Botanic Garden in Ghent, Belgium.[60]

A cultivar of the artificial cross N. bicalcarata × N. × dyeriana was registered in 1988 under the name Nepenthes 'Nina Dodd'. It is named after a relative of Cliff Dodd, who created the hybrid.[61]

Two further cultivars of manmade hybrids involving N. bicalcarata have been named. These are Nepenthes 'Bella' ((N. ampullaria × N. bicalcarata) × N. truncata) and Nepenthes 'Rapa' (N. ampullaria × N. bicalcarata).[62] However, both of these names are not established, as they were published without a description.[5]

References

  1. ^ a b Hooker, J.D. 1873. Nepenthaceae. In: A. de Candolle Prodromus Systematis Naturalis Regni Vegetabilis 17: 90–105.
  2. ^ a b Moore, S.L.M. 1880. Alabastra diversa. The Journal of Botany 18: 1–8.
  3. ^ a b c d e f Phillipps, A. & A. Lamb 1996. Pitcher-Plants of Borneo. Natural History Publications (Borneo), Kota Kinabalu.
  4. ^ a b c d e Bazile, V., J.A. Moran, G. Le Moguédec, D.J. Marshall & L. Gaume 2012. A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism. PLoS ONE 7(5): e36179. doi:10.1371/journal.pone.0036179
  5. ^ a b c Schlauer, J. 2006. Nepenthes bicalcarata. Carnivorous Plant Database.
  6. ^ Jebb, M.H.P. & M.R. Cheek 1997. A skeletal revision of Nepenthes (Nepenthaceae). Blumea 42 (1): 1–106.
  7. ^ Specimen detail: Teijsmann 10962. Nationaal Herbarium Nederland.
  8. ^ Burbidge, F.W. 1882. Notes on the new Nepenthes. The Gardeners' Chronicle 17(1): 56.
  9. ^ Beccari, O. 1896. Malesia, III (1886–1890): Rivista delle specie del genere Nepenthes, p. 1–15.
  10. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z Clarke, C.M. 1997. Nepenthes of Borneo. Natural History Publications (Borneo), Kota Kinabalu.
  11. ^ [Anonymous] 1881. Messr's Veitch's Nepenthes House. The Gardeners' Chronicle n. ser. 16: 598.
  12. ^ Steiner, H. 2002. Borneo: Its Mountains and Lowlands with their Pitcher Plants. Toihaan Publishing Company, Kota Kinabalu.
  13. ^ Danser, B.H. 1928. 4. Nepenthes bicalcarata. In: The Nepenthaceae of the Netherlands Indies. Bulletin du Jardin Botanique de Buitenzorg, Série III, 9(3–4): 249–438.
  14. ^ Cheek, M.R. & M.H.P. Jebb 2001. Nepenthaceae. Flora Malesiana 15: 1–157.
  15. ^ Macfarlane, J.M. 1908. Nepenthaceae. In: A. Engler Das Pflanzenreich IV, III, Heft 36: 1–91.
  16. ^ Adam, J.H. & C.C. Wilcock 1999. Template:PDFlink Pertanika Journal of Tropical Agricultural Science 22(1): 1–7.
  17. ^ Hallier, H. 1895. Ein neues Cypripedium aus Borneo. Natuurkundig Tijdschrift voor Nederlandsch Indië LIV: 450–452.
  18. ^ Schnell, D., P. Catling, G. Folkerts, C. Frost, R. Gardner, et al. 2000. Nepenthes bicalcarata. 2006 IUCN Red List of Threatened Species. IUCN 2006. Retrieved on 11 May 2006. Listed as Vulnerable (VU B1+2c v2.3).
  19. ^ Simpson, R.B. 1995. Nepenthes and conservation. Curtis's Botanical Magazine 12: 111–118.
  20. ^ Merbach, M.A., G. Zizka, B. Fiala, D. Merbach & U. Maschwitz 1999. Template:PDFlink Ecotropica 5: 45–50.
  21. ^ Clarke, C.M. 2001. A Guide to the Pitcher Plants of Sabah. Natural History Publications (Borneo), Kota Kinabalu.
  22. ^ a b Clarke, C.M. & C.C. Lee 2004. Pitcher Plants of Sarawak. Natural History Publications (Borneo), Kota Kinabalu.
  23. ^ a b Dodd, C. 1982. Template:PDFlink Carnivorous Plant Newsletter 11(3): 64–65, 73, 78.
  24. ^ a b c Clarke, C.[M.] 1993. Template:PDFlink Carnivorous Plant Newsletter 22(1–2): 27–28.
  25. ^ Lee, C.C., Hernawati & P. Akhriadi 2006. Two new species of Nepenthes (Nepenthaceae) from North Sumatra. Blumea 51(3): 561–568.
  26. ^ a b Bohn, H.F. & W. Federle 2004. Template:PDFlink Proceedings of the National Academy of Sciences 101(39): 14138–14143.
  27. ^ a b c Moran, J.A., B.J. Hawkins, B.E. Gowen & S.L. Robbins 2010. Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. Journal of Experimental Botany 61(5): 1365–1374. doi:10.1093/jxb/erq004
  28. ^ Di Giusto, B., M. Guéroult, N. Rowe & L. Gaume 2009. Chapter 7: The Waxy Surface in Nepenthes Pitcher Plants: Variability, Adaptive Significance and Developmental Evolution. In: S.N. Gorb (ed.) Functional Surfaces in Biology: Adhesion Related Phenomena. Volume 2. Springer. pp. 183–204.
  29. ^ a b c Moran, J.A., W.E. Booth & J.K. Charles 1999. Template:PDFlink Annals of Botany 83: 521–528.
  30. ^ Shelford, R. 1916. A Naturalist in Borneo. T. Fisher Unwin, London.
  31. ^ Cresswell, J.E. 2000. Resource input and the community structure of larval infaunas of an eastern tropical pitcher plant Nepenthes bicalcarata. Ecological Entomology 25(3): 362–366. doi:10.1046/j.1365-2311.2000.00267.x
  32. ^ Merbach, M.A., G. Zizka, B. Fiala, U. Maschwitz & W.E. Booth 2000. Carnivory and myrmecophytism—a contradiction? Studies on Nepenthes bicalcarata Hook.f. and its ants. Tagungsband gtö 2000 13. Jahrestagung der Deutschen Gesellschaft für Tropenökologie 1–3. March 2000 in Würzburg Lehrstuhl für Tierökologie und Tropenbiologie Universität Würzburg. p. 106.
  33. ^ Schuitemaker, J.P. & A. Stärcke 1933. Contribution a l'etude de la faune Nepenthicole. Art. III Un noveau Camponotus de Borneo, habitant les tiges cruises de Nepenthes récolté par J. P. Schuitemaker et décrit par A. Stärke, den Dolder. Overdruk uit het Natuurhistorisch Maandblad 22(3): 29–31.
  34. ^ Burbidge, F.W. 1880. The Gardens of the Sun: or, a Naturalist's Journal on the Mountains and in the Forests and Swamps of Borneo and the Sulu Archipelago. John Murray, London.
  35. ^ Beccari, O. 1904. Wanderings in the Great Forests of Borneo. Archibald and Constable, London.
  36. ^ Hölldobler, B. & E.O. Wilson 1990. The Ants. Springer-Verlag, Berlin, Germany.
  37. ^ Clarke, C.M. 1992. The ecology of metazoan communities in Nepenthes pitcher plants in Borneo, with special reference to the community of Nepenthes bicalcarata Hook.f. Ph.D. thesis, University of New England, Armidale, New South Wales. 269 pp.
  38. ^ Clarke, C.M. 1998. Initial colonisation and prey capture in Nepenthes bicalcarata (Nepenthaceae) pitchers in Brunei. Sandakania 12: 27–36.
  39. ^ Clarke, C.M. 1998. The aquatic arthropod community of the pitcher plant, Nepenthes bicalcarata (Nepenthaceae) in Brunei. Sandakania 11: 55–60.
  40. ^ Clarke, C.M. & R.L. Kitching 1993. The metazoan food webs from six Bornean Nepenthes species. Ecological Entomology 18(1): 7–16. doi:10.1111/j.1365-2311.1993.tb01074.x
  41. ^ Clarke, C.M. & R.L. Kitching 1995. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. Journal of Tropical Ecology 11(4): 589–602. doi:10.1017/S0266467400009160
  42. ^ Wrenn, E. 2012. How a carnivorous, insect-eating plant has a colony of ANTS to function as a digestive system. Daily Mail, May 10, 2012.
  43. ^ a b c d Bonhomme, V., I. Gounand, C. Alaux, E. Jousselin, D. Barthélémy & L. Gaume 2011. Template:PDFlink Journal of Tropical Ecology 27: 15–24. doi:10.1017/S0266467410000532
  44. ^ Template:Fr icon Gaume, L. N.d. Piège mutualiste. [video] UMR AMAP.
  45. ^ Thompson, J.H. 1981. Reverse animal-plant interactions: the evolution of insectivorous and ant-fed plants. Biological Journal of the Linnean Society 16: 147–155.
  46. ^ Bohn, H.F., D.G. Thornham & W. Federle 2012. Ants swimming in pitcher plants: kinematics of aquatic and terrestrial locomotion in Camponotus schmitzi. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, published online on April 17, 2012. doi:10.1007/s00359-012-0723-4
  47. ^ de Lange, C. 2012. Zoologger: The ant that dives into digestive juices. New Scientist, April 26, 2012.
  48. ^ Hansen, E. 2001. Where rocks sing, ants swim, and plants eat animals: finding members of the Nepenthes carnivorous plant family in Borneo. Discover 22(10): 60–68.
  49. ^ Thornham, D.G., J.M. Smith, T.U. Grafe & W. Federle 2012. Setting the trap: cleaning behaviour of Camponotus schmitzi ants increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata. Functional Ecology 26(1): 11–19. doi:10.1111/j.1365-2435.2011.01937.x
  50. ^ Merbach, M.A., G. Zizka, B. Fiala, D.J. Merbach, W.E. Booth & U. Maschwitz 2007. Template:PDFlink Ecotropica 13: 45–56.
  51. ^ Merbach, M.A. & D.J. Merbach 2002. Template:PDFlink Forschung Frankfurt 2002(3): 74–77.
  52. ^ Choi, C. 2012. Carnivorous plants employ bodyguard ants. LiveScience, May 9, 2012.
  53. ^ Steadman, I. 2012. Carnivorous plants offer ants shelter in return for faeces and protection. Wired, May 10, 2012.
  54. ^ Clarke, C.M. 1997. The effects of pitcher dimorphism on the metazoan community of the carnivorous pitcher plant Nepenthes bicalcarata Hook.f.. Malayan Nature Journal 50: 149–157.
  55. ^ Fashing, N.J. & T.H. Chua 2002. Template:PDFlink International Journal of Acarology 28(2): 157–167.
  56. ^ McPherson, S.R. 2009. Pitcher Plants of the Old World. 2 volumes. Redfern Natural History Productions, Poole.
  57. ^ Hotta, M. 1966. Notes on Bornean Plants. Acta Phytotaxonomica et Geobotanica 22(1–2): 7–9.
  58. ^ D'Amato, P. 1998. The Savage Garden: Cultivating Carnivorous Plants. Ten Speed Press, Berkeley.
  59. ^ Rischer, H. 2000. Growing Nepenthes in a Completely Inorganic Substrate. Carnivorous Plant Newsletter 29(2): 50–53.
  60. ^ Cook, D., J.H. Hummer, A. Vogel, O. Gluch & C. Clayton 2004. New Cultivars. Carnivorous Plant Newsletter 33(1): 19–22.
  61. ^ Robinson, J.T. 1988. New Cultivars. Carnivorous Plant Newsletter 17(1): 20.
  62. ^ Fukatsu, Y. 1999. List of Nepenthes Hybrids.

Further reading

External links

Wikimedia Commons has media related to Nepenthes bicalcarata.
Wikispecies has information related to Nepenthes bicalcarata.

Template:Link GA

Retrieved from "https://en.wikipedia.org/w/index.php?title=Nepenthes_bicalcarata&oldid=492218253"