Abstract
Carnivorous plants avoid below-ground competition for nitrogen by utilizing an alternative nitrogen resource—invertebrate prey, but it remains unclear if sympatric carnivorous plants compete for prey resources. The aim of this study was to investigate if exploitative prey-resource competition occurs between the two sympatric pitcher plant species, Nepenthes rafflesiana and N. gracilis in Singapore. We first investigated if prey-resource partitioning occurs between these two species, and then investigated niche shift in N. gracilis by examining its pitcher contents along an in situ gradient of N. rafflesiana interspecific competition. Our results showed clear evidence of resource partitioning between the two species, but contrary to the expectation of competition, proximity to N. rafflesiana pitchers correlated with higher total prey numbers in N. gracilis pitchers. Our multivariate model of prey assemblages further suggested that N. rafflesiana facilitates N. gracilis prey capture, especially in several ant taxa that are trapped by both species. Concurrently, we found strong evidence for intraspecific competition between N. gracilis pitchers, suggesting that prey resources are exhaustible by pitcher-predation. Our results show that resource partitioning can be associated with facilitative interactions, instead of competition as is usually assumed. Facilitation is more typically expected between phylogenetically distant species, but divergences in resource acquisition strategies can permit facilitation between congeners.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler PB, HilleRislambers J, Levine JM (2007) A niche for neutrality. Ecol Lett 10:95–104. https://doi.org/10.1111/j.1461-0248.2006.00996.x
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525
Bartoń K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bauer U, Federle W, Seidel H, Grafe TU, Ioannou CC (2015) How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants. Proc Biol Sci. https://doi.org/10.1098/rspb.2014.2675
Bauer U, Rembold K, Grafe TU (2016) Carnivorous Nepenthes pitcher plants are a rich food source for a diverse vertebrate community. J Nat Hist. https://doi.org/10.1080/00222933.2015.1059963
Beltran E, Valiente-Banuet A, Verdu M (2012) Trait divergence and indirect interactions allow facilitation of congeneric species. Ann Bot 110:1369–1376. https://doi.org/10.1093/aob/mcs089
Bolton B (1994) Identification guide to the ant genera of the world. Harvard University Press, Cambridge
Bonato KO, Fialho CB (2014) Evidence of niche partitioning under ontogenetic influences among three morphologically similar siluriformes in small subtropical streams. PLoS ONE 9:1–12. https://doi.org/10.1371/journal.pone.0110999
Bonhomme V, Pelloux-Prayer H, Jousselin E, Forterre Y, Labat JJ, Gaume L (2011) Slippery or sticky? functional diversity in the trapping strategy of Nepenthes carnivorous plants. New Phytol 191:545–554. https://doi.org/10.1111/j.1469-8137.2011.03696.x
Bulleri F, Bruno JF, Silliman BR, Stachowicz JJ (2016) Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct Ecol 30:70–78. https://doi.org/10.1111/1365-2435.12528
Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference. Springer-Verlag, New York
Callaway RM, Nadkarni NM, Mahall BE (1991) Facilitation and interference of Quercus douglasii on understory productivity in Central California. Ecol Soc Am 72:1484–1499. https://doi.org/10.2307/1941122
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. https://doi.org/10.1146/annurev.ecolsys.31.1.343
Chin L, Chung A, Clarke C (2014) Interspecific variation in prey capture behavior by co-occurring Nepenthes pitcher plants: evidence for resource partitioning or sampling-scheme artifacts? Plant Signal Behav 9:1–16
Clarke CM (1997) Nepenthes of Borneo. Natural History Publications (Borneo), Kota Kinabalu
Core Team R (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Di Giusto B, Grosbois V, Fargeas E, Marshall DJ, Gaume L (2008) Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from Borneo. J Biosci 33:121–136
Di Giusto B, Bessière JM, Guéroult M, Lim LBL, Marshall DJ, Hossaert-McKey M, Gaume L (2010) Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. J Ecol 98:845–856. https://doi.org/10.1111/j.1365-2745.2010.01665.x
Ellison AM, Gotelli NJ (2003) Evolutionary ecology of carnivorous plants. Trends Ecol Evol 16:623–629. https://doi.org/10.1016/S0169-5347(01)02269-8
Gaume L, Bazile V, Huguin M, Bonhomme V (2016) Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species. Ecol Evol. https://doi.org/10.1002/ece3.1920
Gause GF (1934) The Struggle for existence. Williams and Wilkins, Baltimore
Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution Press, Washington
Gotelli NJ, Hart EM, Ellison AM (2015) EcoSimR: null model analysis for ecological data. Zenodo. https://doi.org/10.5281/zenodo.16636
Goulet H, Huber JT (eds) (1993) Hymenoptera of the world: an identification guide to families. Agriculture Canada Publication
Hui FKC (2016) Boral—Bayesian Ordination and Regression analysis of multivariate abundance data in R. Methods Ecol Evol 7:744–750. https://doi.org/10.1111/2041-210X.12514
Hutchinson GE (1957) Concluding remarks. Cold spring harbor symposia on quantitative biology., pp 415–427
Joel DM (1988) Mimicry and mutualism in carnivorous pitcher plants (Sarraceniaceae, Nepenthaceae, Cephalotaceae, Bromeliaceae). Biol J Linn Soc 35:185–197. https://doi.org/10.1111/j.1095-8312.1988.tb00465.x
Marshall SA (2012) Flies: the natural history and diversity of diptera. In: Firefly books
Mazerolle MJ (2016) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.1-0. https://cran.r-project.org/package=AICcmodavg
McPherson S (2009) Pitcher plants of the old world (2 vols.). In: Redfern Natural History Productions. Poole, Dorset
Montaña CG, Winemiller KO (2013) Evolutionary convergence in Neotropical cichlids and Nearctic centrarchids: evidence from morphology, diet, and stable isotope analysis. Biol J Linn Soc 109:146–164. https://doi.org/10.1111/bij.12021
Moran A (1996) Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. J Ecol 84:515–525
Moran J, Booth W, Charles J (1999) Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture. Ann Bot 83:521–528. https://doi.org/10.1006/anbo.1999.0857
Moran J, Clarke C, Hawkins B (2003) From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. Int J Plant Sci 164:635–639
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Agner H (2016) vegan: Community ecology package. R package version 2.4-1. https://CRAN.R-project.org/package=vegan
Ovaskainen O, Abrego N, Halme P, Dunson D (2016) Using latent variable models to identify large networks of species-to-species associations at different spatial scales. Methods Ecol Evol 7:549–555. https://doi.org/10.1111/2041-210X.12501
Pavlovič A, Saganová M (2015) A novel insight into the cost-benefit model for the evolution of botanical carnivory. Ann Bot 115:1075–1092. https://doi.org/10.1093/aob/mcv050
Pavlovič A, Slováková L, Šantrůček 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
Pianka ER (1974) Niche Overlap and diffuse competition. Proc Natl Acad Sci 71:2141–2145. https://doi.org/10.1073/pnas.71.5.2141
Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160
Rentz DC (2014) A Guide to the cockroaches of australia. Csiro Publishing, Clayton
Rostás M, Tautz J (2010) Ants as Pollinators of Plants and the Role of Floral Scents. In: Dubinsky Z, Seckbach J (eds) All flesh is grass. Cellular origin, life in extreme habitats and Astrobiology, vol 16. Springer, Dordrecht, pp 149–161
Roth LM (1991) Blattodea, Blattaria (cockroaches). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradberry JP, Taylor RW, Whitten MJ, Littlejohn MJ (eds) Insects of Australia: a textbook for students and research workers, vol I. Melbourne University Press, Carlton, pp 320–329
Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611. https://doi.org/10.1016/j.tree.2004.09.003
Sim JWS, Tan HTW, Turner IM (1992) Adinandra belukar: an anthropogenic heath forest in Singapore. Vegetatio 102:125–137. https://doi.org/10.1007/BF00044729
Tan MK (2012a) Orthoptera in the Bukit timah and central catchment nature reserves (part 1): suborder caelifera. Raffles Museum of Biodiversity Research, National University of Singapore, Singapore
Tan MK (2012b) Orthoptera in the Bukit timah and central catchment nature reserves (part 2): suborder ensifera. Raffles Museum of Biodiversity Research, National University of Singapore, Singapore
Tan HTW, Tan WK, Wong CL (1997) Native species and hybrids: tropical pitcher plants. In: Tan HTW (ed) A guide to the carnivorous plants of singapore. Singapore Science Centre, Singapore, pp 51–96
Valiente-Banuet A, Verdú M (2007) Facilitation can increase the phylogenetic diversity of plant communities. Ecol Lett 10:1029–1036. https://doi.org/10.1111/j.1461-0248.2007.01100.x
Volkova Pa, Sukhov ND, Petrov PN (2010) Three carnivorous plant species (Drosera spp.) in European Russia: peaceful coexistence? Nord J Bot 28:409–412. https://doi.org/10.1111/j.1756-1051.2010.00847.x
Walker SC, Jackson DA (2011) Random-effects ordination: describing and predicting multivariate correlations and co-occurrences. Ecol Monogr 81:635–663. https://doi.org/10.1890/11-0886.1
Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101. https://doi.org/10.1111/j.2041-210X.2011.00127.x
Warton DI, Foster SD, De G, Stoklosa J, Dunstan PK (2015) Model-based thinking for community ecology. Plant Ecol. https://doi.org/10.1007/s11258-014-0366-3
Acknowledgements
We thank the following individuals for their advice and/or assistance with prey identification: Tan Ming Kai, for the Orthoptera; Ang Yuchen, for the Diptera; John Ascher and Chui Shao Xiong, for the Aculeata; Lee Yueying and Rachel Lim, for the Araneae; Shingo Hosoishi, Seiki Yamane and Eunice Soh, for the Formicidae; Christina Painting and James Koh, for the Opiliones and Anuj Jain and Gan Cheong Weei, for the Lepidoptera. We are grateful also to Stacey Liang and Ester Suen for their assistance in sample collection; and Francis Hui, for technical advice concerning the R package ‘boral’. We thank also Lai Hao Ran and Roman Carrasco for their constructive comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Anna R. Armitage.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lam, W.N., Wang, W.Y., Cheong, L.F. et al. Pitcher plant facilitates prey capture in a sympatric congener. Plant Ecol 219, 299–311 (2018). https://doi.org/10.1007/s11258-018-0796-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-018-0796-4