Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Comparative anatomy of the assimilatory organs of Nepenthes species

Olusegun O. Osunkoya A B C and Nurul Amal Muntassir A
+ Author Affiliations
- Author Affiliations

A Department of Biology, Universiti Brunei Darussalam, Jalan Tungku Link, Gadon, Bander Seri Begawan, Brunei.

B Invasive Plant and Animal Science Group, Queensland Department of Agriculture and Fisheries, EcoSciences Precinct, Dutton Park, Brisbane, Qld 4001, Australia.

C Corresponding author. Email: Olusegun.osunkoya@daf.qld.gov.au

Australian Journal of Botany 65(1) 67-79 https://doi.org/10.1071/BT16157
Submitted: 4 August 2016  Accepted: 15 December 2016   Published: 20 January 2017

Abstract

There is a lack of data on comparative anatomy of the assimilatory organs of the enigmatic carnivorous Nepenthes species; the linkages between their leaf tissue anatomy and physico-chemical properties are also rarely considered. We examined the anatomy of the leaf (lamina) and its conjoint pitcher in five Nepenthes species (Nepenthes ampullaria, N. bicalcarata, N. gracilis, N. hemsleyana and N. rafflesiana). A Nepenthes leaf displays the usual cuticle–epidermis–hypodermis–palisade–spongy structure with ample stomata distribution for gas exchange. The conjoint pitcher has similar anatomy but lacks a palisade mesophyll layer, and its inner epidermal wall is endowed with digestive glands of three cell layers. A higher level of variation exists in the anatomy of the pitcher relative to the leaf. Both stomata and digestive glands, being similar in origin, display the usual negative log–log relationship between size and density. Across species, the mean size but not density of the glands varied across three readily identified zones of the digestive section of the pitcher. Leaf and pitcher thicknesses correlated (P < 0.05) with stomatal and digestive-gland sizes. Organ longevity, lignin content and construction cost negatively correlated with lower cuticle, epidermal and mesophyll dimensions, and positively so with stomatal and digestive-gland densities. In contrast, major nutrients of N, P, K, and total ash had minimal influence on anatomical size dimensions. It is likely that in Nepenthes leaf and its conjoint pitcher, both the protective and physiological tissues drive anatomical differences and organ functions. The observed bivariate relationships between the anatomical traits also fit into the worldwide leaf economy spectrum.

Additional keywords: Brunei, carnivorous plants, digestive glands, leaf anatomy, South-east Asia, stomata, trait variation.


References

An C-I, Fukusaki E-I, Kobayashi A (2001) Plasma-membrane H+-ATPases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco. Planta 212, 547–555.
Plasma-membrane H+-ATPases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1CgtrY%3D&md5=f1cf62961c6a2be62c3b1aaf9329b32dCAS |

Bauer U, Bohn HF, Federle W (2008) Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proceedings of the Royal Society of London. Series B, Biological Sciences 275, 259–265.
Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar.Crossref | GoogleScholarGoogle Scholar |

Bazile V, Le Moguédec G, Marshall DJ, Gaume L (2015) Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Annals of Botany 115, 705–716.
Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants.Crossref | GoogleScholarGoogle Scholar |

Beerling D, Kelly C (1996) Evolutionary comparative analyses of the relationship between leaf structure and function. New Phytologist 134, 35–51.
Evolutionary comparative analyses of the relationship between leaf structure and function.Crossref | GoogleScholarGoogle Scholar |

Blonder B, Vasseur F, Violle C, Shipley B, Enquist BJ, Vile D (2015) Testing models for the leaf economics spectrum with leaf and whole-plant traits in Arabidopsis thaliana. AoB Plants 7, plv049
Testing models for the leaf economics spectrum with leaf and whole-plant traits in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Bohn HF, Federle W (2004) Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proceedings of the National Academy of Sciences, USA 101, 14138–14143.
Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosVylsLg%3D&md5=495f711d8aff9afd04c503b7d60130d6CAS |

Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199, 559–570.
Unified changes in cell size permit coordinated leaf evolution.Crossref | GoogleScholarGoogle Scholar |

Chen H, Zhang P, Zhang L, Liu H, Jiang Y, Zhang D, Han Z, Jiang L (2016) Continuous directional water transport on the peristome surface of Nepenthes alata. Nature 532, 85–89.
Continuous directional water transport on the peristome surface of Nepenthes alata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xlsl2gtrw%3D&md5=ab9e236b63f5a306bccbc934de5b0b04CAS |

Clarke C, Lee C’i (2004). ‘Pitcher plants of Sarawak.’ (Natural History Publications: Kota Kinabalu, Sabah, Borneo, Malaysia)

Clarke C, Moran JA (2016) Climate, soils and vicariance: their roles in shaping the diversity and distribution of Nepenthes in Southeast Asia. Plant and Soil 403, 37–51.
Climate, soils and vicariance: their roles in shaping the diversity and distribution of Nepenthes in Southeast Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslWisLvK&md5=00449be19675cc1205fa796757cdaf5aCAS |

Daud SD (2004). Variation in properties and construction costs of leaf and pitcher: patterns within and between eight Nepenthes species of Brunei. BSc Thesis, Universiti Brunei Darussalam, Brunei.

de Boer HJ, Price CA, Wagner‐Cremer F, Dekker SC, Franks PJ, Veneklaas EJ (2016) Optimal allocation of leaf epidermal area for gas exchange. New Phytologist 210, 1219–1228.
Optimal allocation of leaf epidermal area for gas exchange.Crossref | GoogleScholarGoogle Scholar |

Edwards C, Sanson GD, Aranwela N, Read J (2000) Relationships between sclerophylly, leaf biomechanical properties and leaf anatomy in some Australian heath and forest species. Plant Biosystems 134, 261–277.
Relationships between sclerophylly, leaf biomechanical properties and leaf anatomy in some Australian heath and forest species.Crossref | GoogleScholarGoogle Scholar |

Ellison AM (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biology 8, 740–747.
Nutrient limitation and stoichiometry of carnivorous plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s%2FgslKmtw%3D%3D&md5=78d1bfe52408f272d53fbbc6237ace83CAS |

Ellison AM, Adamec L (2011) Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120, 1721–1731.
Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same?Crossref | GoogleScholarGoogle Scholar |

Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, USA 106, 10343–10347.
Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1Giurg%3D&md5=bf80688ca1d85361f8b6f1abc05f800eCAS |

Gorb E, Gorb SN (2009) Functional surfaces in the pitchers of the carnivorous plant Nepenthes alata: A cryo-SEM approach. In ‘Functional surfaces in biology. Vol. 2. Adhesion-related effects’. (Ed. SN Gorb) pp. 205–238. (Springer: Dordrecht, Netherlands)

Gorb E, Gorb SN (2011) The effect of surface anisotropy in the slippery zone of Nepenthes alata pitchers on beetle attachment. Beilstein Journal of Nanotechnology 2, 302–310.
The effect of surface anisotropy in the slippery zone of Nepenthes alata pitchers on beetle attachment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1yktrc%3D&md5=2bbf3919f410600b0bdbe10f2f2677f8CAS |

Gorb E, Kastner V, Peressadko A, Arzt E, Gaume L, Rowe N, Gorb S (2004) Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. The Journal of Experimental Biology 207, 2947–2963.
Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention.Crossref | GoogleScholarGoogle Scholar |

Griffith DM, Quigley KM, Anderson TM (2016) Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in Serengeti. Oecologia 181, 1035–1040.
Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in Serengeti.Crossref | GoogleScholarGoogle Scholar |

Hodgson J, Sharafi M, Jalili A, Díaz S, Montserrat-Martí G, Palmer C, Cerabolini B, Pierce S, Hamzehee B, Asri Y (2010) Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Annals of Botany 105, 573–584.
Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3ks1eksA%3D%3D&md5=fae8aa948f4fdfca2b39435d17e222b5CAS |

Jennings DE, Krupa JJ, Raffel TR, Rohr JR (2010) Evidence for competition between carnivorous plants and spiders. Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 3001–3008.
Evidence for competition between carnivorous plants and spiders.Crossref | GoogleScholarGoogle Scholar |

Kanokratana P, Mhuanthong W, Laothanachareon T, Tangphatsornruang S, Eurwilaichitr L, Kruetreepradit T, Mayes S, Champreda V (2016) Comparative study of bacterial communities in Nepenthes pitchers and their correlation to species and fluid acidity. Microbial Ecology 72, 381–393.
Comparative study of bacterial communities in Nepenthes pitchers and their correlation to species and fluid acidity.Crossref | GoogleScholarGoogle Scholar |

Kitajima K, Poorter L (2010) Tissue‐level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist 186, 708–721.
Tissue‐level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species.Crossref | GoogleScholarGoogle Scholar |

Kröber W, Heklau H, Bruelheide H (2015) Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits. Plant Biology 17, 373–383.
Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits.Crossref | GoogleScholarGoogle Scholar |

Lehmann P, Or D (2015) Effects of stomata clustering on leaf gas exchange. New Phytologist 207, 1015–1025.
Effects of stomata clustering on leaf gas exchange.Crossref | GoogleScholarGoogle Scholar |

Moran JA (1996) Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. Journal of Ecology 84, 515–525.
Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo.Crossref | GoogleScholarGoogle Scholar |

Moran JA, Clarke CM (2010) The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions. Plant Signaling & Behavior 5, 644–648.
The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions.Crossref | GoogleScholarGoogle Scholar |

Moran JA, Merbach MA, Livingston NJ, Clarke CM, Booth WE (2001) Termite prey specialization in the pitcher plant Nepenthes albomarginata: evidence from stable isotope analysis. Annals of Botany 88, 307–311.
Termite prey specialization in the pitcher plant Nepenthes albomarginata: evidence from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Moran JA, Hawkins BJ, Gowen BE, Robbins SL (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, 1365–1374.
Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1Kgu7o%3D&md5=2dae2c435b988845f2be2a8e38480bf3CAS |

Osunkoya OO, Daud SD, Di-Giusto B, Wimmer FL, Holige TM (2007) Construction costs and physico-chemical properties of the assimilatory organs of Nepenthes species in northern Borneo. Annals of Botany 99, 895–906.
Construction costs and physico-chemical properties of the assimilatory organs of Nepenthes species in northern Borneo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1altb4%3D&md5=5de1b709fb6916973ce21b03e5c3d487CAS |

Osunkoya OO, Daud SD, Wimmer FL (2008) Longevity, lignin content and construction cost of the assimilatory organs of Nepenthes species. Annals of Botany 102, 845–853.
Longevity, lignin content and construction cost of the assimilatory organs of Nepenthes species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKqurzP&md5=cc930d928648570e5aa46284c42f2f74CAS |

Osunkoya OO, Boyne R, Scharaschkin T (2014) Coordination and plasticity in leaf anatomical traits of invasive and native vine species. American Journal of Botany 101, 1423–1436.
Coordination and plasticity in leaf anatomical traits of invasive and native vine species.Crossref | GoogleScholarGoogle Scholar |

Owen PT, Lennon KA (1999) Structure and development of the pitchers from the carnivorous plant Nepenthes alata (Nepenthaceae). American Journal of Botany 86, 1382–1390.
Structure and development of the pitchers from the carnivorous plant Nepenthes alata (Nepenthaceae).Crossref | GoogleScholarGoogle Scholar |

Owen PT, Lennon KA, Sant MJ, Anderson AN (1999) Pathways for nutrient transport in the pitchers of the carnivorous plant Nepenthes alata. Annals of Botany 84, 459–466.
Pathways for nutrient transport in the pitchers of the carnivorous plant Nepenthes alata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXms1yhurc%3D&md5=e00ac8a886f7d255e8cfbef9e40e17ecCAS |

Pavlovič A, Saganová M (2015) A novel insight into the cost–benefit model for the evolution of botanical carnivory. Annals of Botany 115, 1075–1092.
A novel insight into the cost–benefit model for the evolution of botanical carnivory.Crossref | GoogleScholarGoogle Scholar |

Pavlovič A, Masarovičová E, Hudák J (2007) Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. Annals of Botany 100, 527–536.
Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes.Crossref | GoogleScholarGoogle Scholar |

Reich PB (2014) The world‐wide ‘fast–slow’plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
The world‐wide ‘fast–slow’plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |

Sack L, Scoffoni C, John GP, Poorter H, Mason CM, Mendez-Alonzo R, Donovan LA (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. Journal of Experimental Botany 64, 4053–4080.
How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SmtLfM&md5=2d6ca88d859c3815c333fa73c02069c0CAS |

Scharmann M, Grafe T (2013) Reinstatement of Nepenthes hemsleyana (Nepenthaceae), an endemic pitcher plant from Borneo, with a discussion of associated Nepenthes taxa. Blumea-Biodiversity, Evolution and Biogeography of Plants 58, 8–12.
Reinstatement of Nepenthes hemsleyana (Nepenthaceae), an endemic pitcher plant from Borneo, with a discussion of associated Nepenthes taxa.Crossref | GoogleScholarGoogle Scholar |

Schulze W, Frommer WB, Ward JM (1999) Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. The Plant Journal 17, 637–646.
Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVSqsrw%3D&md5=8905691ef011c60b46dcb92ccba8b4e3CAS |

Schwallier R, Raes N, Boer HJ, Vos RA, Vugt RR, Gravendeel B (2016) Phylogenetic analysis of niche divergence reveals distinct evolutionary histories and climate change implications for tropical carnivorous pitcher plants. Diversity & Distributions 22, 97–110.
Phylogenetic analysis of niche divergence reveals distinct evolutionary histories and climate change implications for tropical carnivorous pitcher plants.Crossref | GoogleScholarGoogle Scholar |

Shipley B, Lechowicz MJ (2000) The functional co-ordination of leaf morphology, nitrogen concentration, and gas exchange in 40 wetland species. Ecoscience 7, 183–194.
The functional co-ordination of leaf morphology, nitrogen concentration, and gas exchange in 40 wetland species.Crossref | GoogleScholarGoogle Scholar |

Takeuchi Y, Salcher MM, Ushio M, Shimizu-Inatsugi R, Kobayashi MJ, Diway B, Von Mering C, Pernthaler J, Shimizu KK (2011) In situ enzyme activity in the dissolved and particulate fraction of the fluid from four pitcher plant species of the genus Nepenthes. PLoS One 6, e25144
In situ enzyme activity in the dissolved and particulate fraction of the fluid from four pitcher plant species of the genus Nepenthes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yqsr7F&md5=c9f2b57869f8ebb89aa2dbcbbb7a8313CAS |

Thornhill AH, Harper IS, Hallam ND (2008) The development of the digestive glands and enzymes in the pitchers of three Nepenthes species: N. alata, N. tobaica, and N. ventricosa (Nepenthaceae). International Journal of Plant Sciences 169, 615–624.
The development of the digestive glands and enzymes in the pitchers of three Nepenthes species: N. alata, N. tobaica, and N. ventricosa (Nepenthaceae).Crossref | GoogleScholarGoogle Scholar |

Vassilyev A, Muravnik L (1988) The ultrastructure of the digestive glands in Pinguicula vulgaris L.(Lentibulariaceae) relative to their function. I. The changes during maturation. Annals of Botany 62, 329–341.

Vico G, Manzoni S, Palmroth S, Katul G (2011) Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytologist 192, 640–652.
Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFWhsr7F&md5=4544d2878d0cf939d297fdbc3826af29CAS |

Wang R, Huang W, Chen L, Ma L, Guo C, Liu X (2011) Anatomical and physiological plasticity in Leymus chinensis (Poaceae) along large-scale longitudinal gradient in northeast China. PLoS One 6, e26209
Anatomical and physiological plasticity in Leymus chinensis (Poaceae) along large-scale longitudinal gradient in northeast China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGjs7fO&md5=88c673b8c90f0e1c6cdf4a843287815dCAS |

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=65bdb98ffc4be2c488788c424bee9a19CAS |

Zhang S-B, Sun M, Cao K-F, Hu H, Zhang J-L (2014) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS One 9, e84682
Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity.Crossref | GoogleScholarGoogle Scholar |