Nepenthes taxonomy : a plea for consistency.

The genus Nepenthes comprises more than 130 recognized species that occur mainly in Southeast Asia with outlying species scattered across islands in the Pacific and Indian oceans (McPherson, 2011). So-called centres of diversity include the islands of Borneo, Sumatra and the Philippines archipelago.

In the beginning, a handful of species…

Nepenthes were discovered about 350 years ago.

Nepenthes madagascariensis was first described (as Amramatico, a local name) by French Etienne de Flacourt in 1658.

Nepenthes distillatoria

Plukenet’s drawing of N. distillatoria, Almagestum Botanicum, 1696.

First mentionned as Miranda herba in 1677 by Bartholinus.

Cantharifera as published in Rumphius’s Herbarium Amboinensis, 1747.

Bandura zeylanica (N. distillatoria) from Burnmann’s Thesaurus Zeylanicus, 1737.

Nepenthes mirabilis

Described in 1790 as Phyllamphora mirabilis by Joao de Loureiro.

Evolution of Nepenthes species number since the description written by Etienne de Flacourt in 1658.

Major publications: v  Hooker, De Candolle’s Prodomus, 1873: 33 species. v  Macfarlane, Engler’s Planzenreich, 1908: 58 species. v  Danser, The Nepenthaceae of the Netherland Indies, 1928: 65 species. v Jebb & Cheek, A skeletal revision of Nepenthes, 1997: 82 species. v  Clarke, Nepenthes of Borneo and Nepenthes of Sumatra and Peninsular Malaysia, 1997 and 2001: 31 and 34 species in Borneo and Sumatra respectively. v  McPherson: New Nepenthes, 2011: 138 species.

A short gallery of some emblematic species

45 taxa described from 1998 to 2013 (1/2)

N. mira, 1998 (Philippines) N. glandulifera, 2004 (Borneo)

N. sibuyanensis, 1998 (Philippines) N. rigidifolia, 2004 (Sumatra)

N. angasanensis, 1999 (Sumatra) N. chaniana, 2006 (Borneo)

N. benstonei, 1999 (Peninsular Malaysia) N. jamban, 2006 (Sumatra)

N. jacquelinae, 2001 (Sumatra) N. lingulata, 2006 (Sumatra)

N. mindanaoensis, 2001 (Philippines) N. tenax, 2006 (Australia)

N. platychila, 2002 (Borneo) N. flava, 2007 (Sumatra)

N. vogelii, 2002 (Borneo) N. mantalingajanensis, 2007 (Philippines)

N. hurrelliana, 2003 (Borneo) N. peltata, 2008 (Philippines)

N. izumiae, 2003 (Sumatra) N. attenboroughii, 2009 (Philippines)

N. saranganiensis, 2003 (Philippines) N. bokorensis, 2009 (Cambodia)

45 taxa described from 1998 to 2013 (2/2)

N. naga, 2009 (Sumatra)

N. micramphora, 2009 (Philippines)

N. pitopangii, 2009 (Sumatra)

N. thai, 2009 (Thailand)

N. andamana, 2010 (Thailand)

N. chang, 2010 (Thailand)

N. gantungensis, 2010 (Philippines)

N. hamiguitanensis, 2010 (Philippines)

N. holdenii, 2010 (Cambodia)

N. kerrii, 2010 (Thailand)

N. mirabilis var. globosa, 2010(Thailand)

N. palawanensis, 2010 (Philippines)

N. suratensis, 2010 (Thailand)

N. appendiculata, 2011 (Borneo)

N. baramensis, 2011 (Borneo)

N. ceciliae, 2011 (Philippines)

N. epiphytica, 2011 (Borneo)

N. leonardoi, 2011 (Philippines)

N. monticola, 2011 (Papua)

N. nigra, 2011 (Sulawesi)

N. pulchra, 2011 (Philippines)

N. robcantleyi, 2011 (Philippines)

N. undulatifolia, 2011 (Sulawesi)

N. abalata, 2013 (Philippines)

And there’s more…

Taxa that were redefined after rediscovery or new field studies:

N. alba, reinstated in 2009 (Peninsular Malaysia)

N. deaniana, redefined in 2009 (Philippines)

N. lamii , redefined in 2011 (Papua)

N. pilosa, redefined in 2006 (Borneo)

N. rowanae, reinstated in 2005 (Australia)

N. smilesii, redefined in 2009 (whole Indochinese peninsula)

N. surigaoensis, redefined in 2008 (Philippines)

N. thorelii, redefined in 2011 (Vietnam)

Exemples of taxa awaiting formal descriptions:

N. « sp. Anipahan »

N. « sp. Luzon »

N. « sp. Misool »

N. hamata « hairy »

Some explanations to the increasing number of Nepenthes formal descriptions:

v  Nepenthes have broad horticultural appeal.

v  Knowledge of the plants is readily available and circulates faster.

v  Travels and logistics are much easier than in the past, hence botanists and enthusiasts travel extensively through some previously remote areas.

Stewart McPherson (with N. palawanensis).

« Continuing exploration is likely to reveal additional Nepenthes species, as well as information that adds to our understanding of the

diversity, ecology and taxonomy of these complex […] plants »

S. McPherson, New Nepenthes, 2011, p.9.

The question is: should all of these plants (described ones and forthcoming ones) be classified as new « species »?

Danser’s revision (1928) set the standard for Nepenthes taxonomy.

He is the only author to date who attempted a kind of phylogenetic classification within the family: six i n f o r m a l g r o u p s b a s e d o n morphological affinities: Vulgatae, Montanae, Nobiles, Regiae, Insignes and Urceolatae.

Benedictus Hubertus DANSER (1891-1943)

Danser proposed a clear protocol for describing and distinguishing taxa at specific rank. Minor and/or unstable morphological characteristics, such as plant or pitcher size, and variations in colour, were not regarded as significant. As such, N. edwarsiana was reduced as a synonym of N. villosa. Following his view, the two entities would belong to a variable species incuding N. edwarsiana-N. x harryana- and N. villosa (+N. macrophylla).

Danser did not recognize any sub-specific taxa. Danser’s work was very influential; major subsequent taxonomic treatments of the genus followed his approach.

Recent major publications

Basically, since Danser,Nepenthes

taxonomy relies on the study of morphological features of the

plants with characteristics of the

pitchers, inflorescences, leaf blades and indumentum being the most

informative.

Previous to Danser, many infraspecific taxa have been recognized (by Beck, Ridley, Macfarlane,Lindley or Bailey among others) but Danser thought that those earlier taxa did not merit recognition.

« Often authors have gone so far as to describe specimens with extremely large or broad leaves, or with very long internodes, and different stages of growth as varieties or even species. Continuing this way can only discredit systematics,especially that of form within the species. » The Nepenthaceae of the Netherland Indies, p. 250.

«Subspecies and varieties have nowhere been distinguished by me, as the polymorphy of the species in general is too little known to make such a distinction in the same weigh in each case. The forms that deserved a specific name have been given one, the less clearly limited forms have not been named at all. This seems to the right way to avoid complication of the nomenclature of a genus so little known »

The Nepenthaceae of the Netherland Indies, p. 250.

The highly variable N. rafflesiana

The start of departure from Danser’s approach. Danser’s influential work is now 85 years old and our collective knowledge of the genus have significantly increased. Dozens of taxa have been documented in the field. « Lost » species have been rediscovered. 2006: Clarke and Moran described N. tenax, a taxon very closely related to N. mirabilis.

N. mirabilis N. tenax

In the last years, several new species have been delimited, separated from others, using morphological characteristics that Danser would have deemed

irrelevant.

Here are some species that Danser might not have recognized:

N. leonardoi

N. gantungensis

N. deaniana

N. mira

N. mantalingajanensis

N. petiolata N. pulchra

andamana

andamana

bokorensis

bokorensis

chang

chang

holdenii

holdenii

kampotiana

kampotiana

kerrii

kerrii

smilesii

smilesii

suratensis

suratensis

thorelii

thorelii

bokorensis

Currently, a lack of consistency?

N. rowanae (or « N. mirabilis var. rowanae »?) N. mirabilis var. globosa (or « N. globosa »)?

Aggregates, complexes or sub-groups have to be solved out:

-Nepenthes bongso aggregates;

-Nepenthes deaniana aggregate; -Nepenthes mirabilis aggregate;

-Nepenthes alata aggregate; -Nepenthes singalana aggregate;

-Nepenthes thorelii aggregate.

To some (Clarke, 2011), current trend is reminiscent of the late 1800s with taxa that were not clearly delimitated. This led to confusion among taxonomists and

horticulturists. Is this happening again?

The status of some of the new (and old) species may appear controversial with a number being distinguished from others on the basis of apparently minor morphological

characteristics that may not be stable.

Highly variable species? Dozens of very closely related species?

Or something else?

It would be an oversimplification to assume that all taxa within each of those aggregates are the same because of their common traits. But they arguably deserve better study so as to better characterize each of them and their relations. Only two varieties are recognized: N. mirabilis var. echinostoma and N. mirabilis var. globosa.

Why?

What impedes accurate Nepenthes taxonomy? v  Variety of species and subspecies concepts;

v  Nothotaxa;

v  Interpretations based on limited herbarium material;

v  A lack of field studies,

v  Danser’s influence,

v  Egos…

In Linnean classification: v  Subspecies should develop differences that are less distinct that between species. Ssp. are often isolated geographically.

v  Variety should differ from species by minor but stable characteristics . v  Forma develop a single or a few very minor characteristics.

The subspecific rank is generally applied when there is indecision if a taxa is a different species or a variety. A subspecies can also be seen as a taxon on in its way to speciation.

The use of infraspecific ranks?

Maybe it is time that Nepenthes taxonomists agree on the standards for species and subspecies

designation?

Hints?

v  Morphological characteristics backed up with extensive field studies. v  Molecular studies (« in progress » cf Meimberg et al., 2001). v  Ecology.

Enhancing the value of ecological datas

These last years, it became apparent to ecologists that the degree of development of the peristome, waxy zone as well as geometry trap are fundamental to the prey

strategies of many Nepenthes species: N. bicalcarata, N. gracilis, N. inermis, N. jacquelinae, N. rafflesiana…

Solving a debate with the help of ecology: the exemple of N. macrophylla.

N. macrophylla was first described as a ssp. of N. edwarsiana (Marabini) then, it was elevated to the species rank (Jebb & Cheek) but there were still some reservations.

If we knew that N. macrophylla belongs to a group of three Bornean species

feeding on tree shrew faeces, the case would have been closed earlier. The tree shrew Tupaia montana clearly distinguishes N. macrophylla from N. edwarsiana or N. villosa.

N. baramensis : an exemple of a species delimited by ecology.

This taxon was circumscribed mainly based on its ecological feature: its mutualistic relationship with a bat species (Kerivoula hardwickii) BUT: N. baramensis can barely be separated from its closest relative N. rafflesiana from a morphological point of view.

Emphasize the study of wild plants

N. thorelii in situ, southern Vietnam.

While collecting and pressing a Nepenthes…

…record as much ecological informations as possible.

Suggestions for pressing and mounting collections of Nepenthes:

For full detailed protocol, see:

Clarke C., J. A. Moran,

Incorporating ecological context : a revised protocol for the preservation of Nepenthes pitcher plant specimens (Nepenthaceae), Blumea 56, 2011: 225-228.

-"try to preserve the angle of lid reflexion and concavity/convexity of the lids. If the lid angle cannot be faithfully preserved, indicate on the label what the approximate, typical angle of lid reflexion is, for both lower and upper pitchers; -Preservation of pitchers in alcohol can be an effective method of preserving trap geometry. Alternatively (and particularly for very large pitchers) a series of high-quality photographs that accurately depict trap geometry will serve a similar purpose; -The habitat in which the material was collected (e.g. forest type, altitude, substrate);

-Observations about conspicuous animal visitors to both the pitchers and the inflorescences (invertebrates and vertebrates); -Features unlikely to be obvious in preserved material (e.g. fragrance produced by pitchers (specify upper or lower form) or inflorescences (specify sex); viscosity of pitcher fluid (specify upper or lower form); -If possible, the contents of one upper and one lower pitcher should be extracted, dried and attached to the card in a clearly labeled, paper envelope."

Sub-adult praying mantis from the genus Creobroter on the inflorescence of N. thorelii.

Conclusions

v  Nepenthes taxonomy is not accurate enough.

v  The urge do delimitate guideline for the descriptions of new species,

subspecies and varieties (even formas).

v  The need to reclassify some of the existing taxa, reducing thus the number of species but helping to have a better understanding of the species relationships.

v  We need a new revision!

Thank you for your

attention!