Diversity and volume of international trade in Old World pitcher plants
Irena Šetlíková A B and Michal Berec AA Faculty of Agriculture, University of South Bohemia, Studentská 1668, CZ-370 05 České Budějovice, Czech Republic. Email address: michal.berec@seznam.cz
B Corresponding author. Email address: setlik@zf.jcu.cz
Australian Journal of Botany 68(5) 376-383 https://doi.org/10.1071/BT20027
Submitted: 13 March 2020 Accepted: 27 August 2020 Published: 20 October 2020
Abstract
In global trade analyses, plants are neglected in comparison to animals. Controlling and monitoring international trade in threatened species contributes to their overall conservation. Here, an in-depth look at the dynamics of the international trade in attractive and widely traded carnivorous Old World pitcher plants (Nepenthes spp.) from their first appearance in the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) Trade Database in 1983 until 2017 is presented. The current trade of Nepenthes is rapidly growing in terms of the total volume traded and the number of both species and importing countries. Most of pitcher plants are globally traded as artificially propagated live plants. The share of wild-originated live plants was only 0.09%. Hybrids and Nepenthes spp. dominated the trade, representing 61 and 15% of the total traded volume respectively, followed by N. alata and N. mirabilis. The latter species was also the most traded species from the wild. Sri Lanka is a hotspot, exporting the highest volume and number of species of live pitcher plants. Monitoring of the trade is complicated by (1) the absence of a permit obligation for seeds, seedlings and in vitro cultures, and (2) the outdated list of valid species in the CITES Checklist. Using a holistic approach with a focus on the permanent monitoring, recording and assessing of international trade is desirable.
Keywords: carnivorous plants, CITES, Convention on International Trade in Endangered Species of Wild Flora and Fauna, inventory and monitoring, Nepenthes, wildlife trade.
References
Averyanov L, Cribb P, Loc PK, Hiep NT (2003) ‘Slipper Orchids of Vietnam: With an Introduction to the Flora of Vietnam.’ (Timber Press: Portland, OR, USA)Berec M, Šetlíková I (2019) Important step to understanding the CITES Trade Database: a reply to Pavitt et al. Biological Conservation 230, 197–198.
| Important step to understanding the CITES Trade Database: a reply to Pavitt et al.Crossref | GoogleScholarGoogle Scholar |
Berec M, Vršecká L, Šetlíková I (2018) What is the reality of wildlife trade volume? CITES Trade Database limitations. Biological Conservation 224, 111–116.
| What is the reality of wildlife trade volume? CITES Trade Database limitations.Crossref | GoogleScholarGoogle Scholar |
CITES (2013) A guide to using the CITES trade database. (CITES: Cambridge, UK) Available at https://trade.cites.org/cites_trade_guidelines/en-CITES_Trade_Database_Guide.pdf [Verified 3 August 2019]
CITES (2019) Global trade in plants (excluding cacti and orchids). (CITES: Cambridge, UK) Available at http://dashboards.cites.org/global?id=Plants%20%28excluding%20cacti%20%26%20orchids%29 [Verified 26 November 2019]
CITES (2020) CITES appendices I, II, III valid from 26.11.2019. (CITES: Cambridge, UK) Available at https://www.cites.org/eng/app/appendices.php [Verified 12 March 2020]
Clarke C (1997) ‘Nepenthes of Borneo.’ (Natural History Publications (Borneo): Kota Kinabalu, Borneo)
Clarke C (2001) ‘Nepenthes of Sumatra and Peninsular Malaysia.’ (Natural History Publications (Borneo): Kota Kinabalu, Borneo)
Clarke C (2014) Nepenthes mirabilis. In ‘The IUCN Red List of Threatened Species 2014’. e.T49122515A21844202. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK) Available at https://www.iucnredlist.org/species/49122515/21844202 [Verified 15 November 2019]
Clarke C, Cantley R, Nerz J, Rischer H, Witsuba A (2000) Nepenthes distillatoria. In ‘The IUCN Red List of Threatened Species 2000’. e.T39656A10254604. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK) Available at https://www.iucnredlist.org/species/39656/10254604 [Verified 5 January 2020]
Clarke CM, Bauer U, Lee Ci C, Tuen AA, Rembold K, Moran JA (2009) Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5, 632–635.
| Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant.Crossref | GoogleScholarGoogle Scholar | 19515656PubMed |
Courchamp F, Angulo E, Rivalan P, Hall RJ, Signoret L, Bull L, Meinard Y (2006) Rarity value and species extinction: the anthropogenic Allee effect. PLoS Biology 4, e415
| Rarity value and species extinction: the anthropogenic Allee effect.Crossref | GoogleScholarGoogle Scholar | 17132047PubMed |
Dormontt EE, Boner M, Braun B, Breulmann G, Degen B, Espinoza E, Gardner S, Guillery P, Hermanson JC, Koch G (2015) Forensic timber identification: it’s time to integrate disciplines to combat illegal logging. Biological Conservation 191, 790–798.
| Forensic timber identification: it’s time to integrate disciplines to combat illegal logging.Crossref | GoogleScholarGoogle Scholar |
Ellison AM, Adamec L (Eds) (2018) ‘Carnivorous Plants: Physiology, Ecology, and Evolution.’ (Oxford University Press: Oxford, UK)
Gale SW, Kumar P, Hinsley A, Cheuk ML, Gao J, Liu H, Liu Z-L, Williams SJ (2019) Quantifying the trade in wild-collected ornamental orchids in South China: diversity, volume and value gradients underscore the primacy of supply. Biological Conservation 238, 108204
| Quantifying the trade in wild-collected ornamental orchids in South China: diversity, volume and value gradients underscore the primacy of supply.Crossref | GoogleScholarGoogle Scholar |
Gaume L, Bazile V, Huguin M, Bonhomme V (2016) Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species. Ecology and Evolution 6, 1378–1392.
| Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species.Crossref | GoogleScholarGoogle Scholar | 26865951PubMed |
Ghosh D, Ghosh S (2012) India’s only pitcher plant in peril. Scientific Reports 2012, 53–56.
Goettsch B, Hilton-Taylor C, Cruz-Piñón G, Duffy JP, Frances A, Hernández HM, Inger R, Pollock C, Schipper J, Superina M (2015) High proportion of cactus species threatened with extinction. Nature Plants 1, 15142
| High proportion of cactus species threatened with extinction.Crossref | GoogleScholarGoogle Scholar | 27251394PubMed |
Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG (2011) A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7, 436–439.
| A novel resource–service mutualism between bats and pitcher plants.Crossref | GoogleScholarGoogle Scholar | 21270023PubMed |
Harfoot M, Glaser SA, Tittensor DP, Britten GL, McLardy C, Malsch K, Burgess ND (2018) Unveiling the patterns and trends in 40 years of global trade in CITES-listed wildlife. Biological Conservation 223, 47–57.
| Unveiling the patterns and trends in 40 years of global trade in CITES-listed wildlife.Crossref | GoogleScholarGoogle Scholar |
Hinsley A, Roberts DL (2018) The wild origin dilemma. Biological Conservation 217, 203–206.
| The wild origin dilemma.Crossref | GoogleScholarGoogle Scholar |
Hinsley A, De Boer HJ, Fay MF, Gale SW, Gardiner LM, Gunasekara RS, Kumar P, Masters S, Metusala D, Roberts DL (2018) A review of the trade in orchids and its implications for conservation. Botanical Journal of the Linnean Society 186, 435–455.
| A review of the trade in orchids and its implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Hua Y, Li H (2005) Food web and fluid in pitchers of Nepenthes mirabilis in Zhuhai, China. Acta Botanica Gallica 152, 165–175.
| Food web and fluid in pitchers of Nepenthes mirabilis in Zhuhai, China.Crossref | GoogleScholarGoogle Scholar |
IUCN (2020) Taxonomy search: Nepenthes – Genus; Geographical Scope: Global; Include: Species. In ‘The IUCN Red List of threatened species’. Version 2019-3. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK) Available at https://www.iucnredlist.org/search?taxonomies=125636&searchType=species [Verified 30 September 2020]
Janssen J, Shepherd CR (2018) Challenges in documenting trade in non CITES-listed species: a case study on crocodile skinks (Tribolonotus spp.). Journal of Asia-Pacific Biodiversity 11, 476–481.
| Challenges in documenting trade in non CITES-listed species: a case study on crocodile skinks (Tribolonotus spp.).Crossref | GoogleScholarGoogle Scholar |
Jennings DE, Rohr JR (2011) A review of the conservation threats to carnivorous plants. Biological Conservation 144, 1356–1363.
| A review of the conservation threats to carnivorous plants.Crossref | GoogleScholarGoogle Scholar |
Kurata S (1976) ‘Nepenthes of Mount Kinabalu.’ (Sabah National Parks Trustees: Kota Kinabalu, Malaysia)
Lavorgna A, Rutherford C, Vaglica V, Smith MJ, Sajeva M (2018) CITES, wild plants, and opportunities for crime. European Journal on Criminal Policy and Research 24, 269–288.
| CITES, wild plants, and opportunities for crime.Crossref | GoogleScholarGoogle Scholar |
Margulies JD, Hinsley A, Phelps J (2018) Illegal wildlife trade endangers plants – but few are listening. In ‘IUCN Blog’. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK) Available at https://www.iucn.org/news/species/201810/illegal-wildlife-trade-endangers-plants-few-are-listening [Verified 15 January 2020]
Margulies JD, Bullough LA, Hinsley A, Ingram DJ, Cowell C, Goettsch B, Klitgård BB, Lavorgna A, Sinovas P, Phelps J (2019) Illegal wildlife trade and the persistence of ‘plant blindness’. Plants, People Planet 1, 173–182.
| Illegal wildlife trade and the persistence of ‘plant blindness’. Plants, PeopleCrossref | GoogleScholarGoogle Scholar |
McPherson S (2009) ‘Pitcher Plants of the Old World.’ (Redfern Natural History Productions: Poole, UK)
Merbach MA, Merbach DJ, Maschwitz U, Booth WE, Fiala B, Zizka G (2002) Mass march of termites into the deadly trap. Nature 415, 36–37.
| Mass march of termites into the deadly trap.Crossref | GoogleScholarGoogle Scholar | 11780106PubMed |
Moran JA, Clarke CM, Hawkins BJ (2003) From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. International Journal of Plant Sciences 164, 635–639.
| From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria.Crossref | GoogleScholarGoogle Scholar |
Murphy B, Forest F, Barraclough T, Rosindell J, Bellot S, Cowan R, Golos M, Jebb M, Cheek M (2020) A phylogenomic analysis of Nepenthes (Nepenthaceae). Molecular Phylogenetics and Evolution 144, 106668
| A phylogenomic analysis of Nepenthes (Nepenthaceae).Crossref | GoogleScholarGoogle Scholar | 31682924PubMed |
Nongrum I, Kumar S, Kumaria S, Tandon P (2012) Genetic variation and gene flow estimation of Nepenthes khasiana Hook.F – a threatened insectivorous plant of India as revealed by RAPD markers. Journal of Crop Science and Biotechnology 15, 101–105.
| Genetic variation and gene flow estimation of Nepenthes khasiana Hook.F – a threatened insectivorous plant of India as revealed by RAPD markers.Crossref | GoogleScholarGoogle Scholar |
Novoa A, Le Roux JJ, Richardson DM, Wilson JR (2017) Level of environmental threat posed by horticultural trade in Cactaceae. Conservation Biology 31, 1066–1075.
| Level of environmental threat posed by horticultural trade in Cactaceae.Crossref | GoogleScholarGoogle Scholar | 28074500PubMed |
Pavlovič A, Slováková Ľ, Šantrůček J (2011) Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria. Plant, Cell & Environment 34, 1865–1873.
| Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria.Crossref | GoogleScholarGoogle Scholar |
Phelps J, Webb EL (2015) ‘Invisible’ wildlife trades: Southeast Asia’s undocumented illegal trade in wild ornamental plants. Biological Conservation 186, 296–305.
| ‘Invisible’ wildlife trades: Southeast Asia’s undocumented illegal trade in wild ornamental plants.Crossref | GoogleScholarGoogle Scholar |
Pietropaolo J, Pietropaolo PA (1997) ‘Carnivorous Plants of the World.’ (Timber Press: Portland, OR, USA)
Robinson JE, Sinovas P (2018) Challenges of analyzing the global trade in CITES-listed wildlife. Conservation Biology 32, 1203–1206.
| Challenges of analyzing the global trade in CITES-listed wildlife.Crossref | GoogleScholarGoogle Scholar | 29455463PubMed |
Roe D (2008) Trading nature: a report, with case studies, on the contribution of wildlife trade management to sustainable livelihoods and the Millennium Development Goals. (TRAFFIC International and WWF International: Cambridge, UK) Available at https://www.traffic.org/publications/reports/trading-nature-the-contribution-of-wildlife-trade-management-to-sustainable-livelihoods-and-the-millennium-development-goals/ [Verified 15 January 2020]
Sajeva M, Carimi F, McGough N (2007) The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and its role in conservation of cacti and other succulent plants. Functional Ecosystems and Communities 1, 80–85.
Scheffers BR, Oliveira BF, Lamb I, Edwards DP (2019) Global wildlife trade across the tree of life. Science 366, 71–76.
| Global wildlife trade across the tree of life.Crossref | GoogleScholarGoogle Scholar | 31604304PubMed |
Seaton K, Bettin A, Grüneberg H (2014) New ornamental plants for horticulture. In ‘Horticulture: Plants for People and Places’. (Eds GR Dixon, DE Aldous) pp. 435–463. (Springer: Dordrecht, Netherlands)
Setiawan H (2017) Nepenthes as tourism flagship species: the conservation strategies in Dayak Seberuang settlements area. Journal of Indonesian Tourism and Development Studies 5, 113–120.
| Nepenthes as tourism flagship species: the conservation strategies in Dayak Seberuang settlements area.Crossref | GoogleScholarGoogle Scholar |
Shepherd CR, Ibarrondo B (2005) ‘The trade of the Roti Island snake-necked turtle Chelodina mccordi, Indonesia.’ (TRAFFIC Southeast Asia: Petaling Jaya, Selangor, Malaysia)
Simpson R (1995) Nepenthes and conservation. Curtis’s Botanical Magazine 12, 111–118.
| Nepenthes and conservation.Crossref | GoogleScholarGoogle Scholar |
Vaglica V, Sajeva M, McGough HN, Hutchison D, Russo C, Gordon AD, Ramarosandratana AV, Stuppy W, Smith MJ (2017) Monitoring internet trade to inform species conservation actions. Endangered Species Research 32, 223–235.
| Monitoring internet trade to inform species conservation actions.Crossref | GoogleScholarGoogle Scholar |
Winter J, Botha D (1994) The release of endangered plants into the horticultural trade: conservation or exploitation? Biodiversity and Conservation 3, 142–147.
| The release of endangered plants into the horticultural trade: conservation or exploitation?Crossref | GoogleScholarGoogle Scholar |