Corresponding author: Llewellyn Jacobs ( email@example.com )
Academic editor: Ingo Kowarik
© 2017 Llewellyn Jacobs, David Richardson, Brendan Lepschi, John Wilson.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Jacobs LEO, Richardson DM, Lepschi BJ, Wilson JRU (2017) Quantifying errors and omissions in alien species lists: The introduction status of Melaleuca species in South Africa as a case study. NeoBiota 32: 89-105. https://doi.org/10.3897/neobiota.32.9842
Introduced species lists provide essential background information for biological invasions research and management. The compilation of these lists is, however, prone to a variety of errors. We highlight the frequency and consequences of such errors using introduced Melaleuca (sensu lato, including Callistemon) species in South Africa as a case study. We examined 111 herbarium specimens from South Africa and noted the categories and sub-categories of errors that occurred in identification. We also used information from herbarium specimens and distribution data collected in the field to determine whether a species was introduced, naturalized and invasive. We found that 72% of the specimens were not named correctly. These were due to human error (70%) (misidentification, and improved identifications) and species identification problems (30%) (synonyms arising from inclusion of Callistemon, and unresolved taxonomy). At least 36 Melaleuca species have been introduced to South Africa, and field observations indicate that ten of these have naturalized, including five that are invasive. While most of the errors likely have negligible impact on management, we highlight one case where incorrect identification lead to an inappropriate management approach and some instances of errors in published lists. Invasive species lists need to be carefully reviewed to minimise errors, and herbarium specimens supported by DNA identification are required where identification using morphological features is particularly challenging.
Biological invasions, Callistemon, herbarium specimen, invasive species listing, Myrtaceae, tree invasions
Species lists form the basis for much of the current research on biological invasions (e.g. the Global Naturalized Alien Flora Database of
For plants, herbaria are indispensable resources and reference sources for much botanical research which requires reliable species identifications, including the compilation of introduced species lists (
The genus Melaleuca has not been distributed around the world as extensively as some other tree groups (e.g. Eucalyptus, a sister genus in the Myrtaceae) (
In 2009, the discovery of several naturalised populations of Melaleuca species in South Africa prompted an evaluation of the introduction status for the entire group in the country (
Here, we compile a list of Melaleuca species recorded as present in South Africa and determine the invasive status of each species. We use herbarium specimens to do this, while also noting the extent to which they are accurately identified and the types of errors which occur. We discuss consequences of errors and omissions and make recommendations on how these could be avoided and addressed.
Generic limits in the tribe Melaleuceae have been the subject of much recent study (
Herbarium specimens from the Compton herbarium (NBG) were examined to check whether specimen identifications were correct, and to provide accurate identifications where necessary. To do this, we used the taxonomic literature to compare morphological characters on the specimens with descriptions and taxonomic keys (in particular
Herbarium specimens were examined in 2013; any specimens accessioned or re-identified after this date were not included in the analysis.
Result of analysis of confirmed herbarium records (n=111), indicating the breakdown of correctly identified specimens with various error types. For full details see Suppl. material
|Status||Description||Number of herbarium specimens||Examples|
|Correctly identified||The identification on the herbarium specimen was the same as determined by an expert in the group (the author: BL)||31||Seven specimens of Melaleuca styphelioides and five specimens of M. hypericifolia correctly identified|
|Misidentification (HE)||The identification on the herbarium specimen was to a currently accepted species, but not the correct one||31||Melaleuca parvistaminea, M. armillaris subsp. armillaris and M. cuticularis were misidentified as M. ericifolia|
|Further identification (HE)||The identification on the herbarium specimen could be refined, either by providing the specific epithet or the subspecific epithet||25||Several specimens (e.g. M. rugulosa) only identified to genus level; M. armillaris could be identified further to subspecies level|
|Unresolved taxonomy (SI)||The taxonomy used to identify the herbarium specimen was not resolved at that time, so any name provided will have some uncertainty around it.||2||Several names misapplied to Melaleuca quinquenervia (prior to 1968)|
|Synonym (SI)||The identification was confirmed, but the name on the herbarium specimen was not the most current accepted name||22||Nine specimens of Callistemon rigidus (a synonym of C. linearis, also a synonym of Melaleuca linearis var. linearis), Callistemon viminalis = Melaleuca viminalis subsp. viminalis|
We also looked to see if there were any historical trends in the errors by comparing the years when taxa with particular errors were collected to the years when taxa with no errors were collected using Mann-Whitney U tests in R.
Once correct identification for all specimens had been confirmed, we used these specimens as the source for compiling a list of species present in South Africa. We also used a list of cultivated plants based on herbarium records in southern Africa (
Naturalized populations were reported by a variety of conservation agencies, with the reports collated by the South African National Biodiversity Institute’s Invasive Species Programme and through the Southern African Plant Invaders Atlas (
We collected height data as an estimate of age, presence/absence of reproductive structures and GPS coordinates for each plant. Using these data we were able to determine whether a species is sustaining itself, whether it is reproducing and/or spreading, hereby indicating the status of each species as introduced, naturalized or invasive according to the subcategories proposed by
A summary of the errors found is in Table
Examples of the types of errors found on the herbarium specimens examined, a Misidentification: Melaleuca salicina misidentified as Callistemon pallidus b Improved identification: Callistemon sp. was further identified as Melaleuca rugulosa c Synonymy: Callistemon rigidus is a synonym of C. linearis but is currently accepted as Melaleuca linearis var. linearis, and d unresolved taxonomy: prior to 1968, Melaleuca quinquenervia, along with several other broad-leaved species were included under M. leucadendra sensu lato.
There was no significant effect of date of collection on whether an error was noted, or on particular errors types (dates of collection varied between 1907 and 2013).
Our analysis of herbarium specimens and the lists in
Examples of naturalized Melaleuca species in South Africa. a naturalized M. quinquenervia plants showing seed capsules opening after fire b M. viminalis subsp. viminalis naturalized along a stream in an urban setting c Melaleuca parvistaminea invading a conservation area that was previously under pine plantation, and d M. linearis var. linearis is invasive at another site previously under plantation with M. parvistaminea in background. Photos: a, c is E van Wyk, b is LEO Jacobs, d is DM Richardson.
Localities of naturalized Melaleuca species in South Africa at the resolution of quarter-degree squares (QDS). Darker shading indicates a higher number of species. Grey borders are province boundaries.
List of 36 Melaleuca species in South Africa for which there is a confirmed herbarium record in either the Compton Herbarium, Kirstenbosch (NBG) or in the cultivated collection in the National Herbarium (PRE). Note that several other collections were searched, but no additional species could be discovered. Invasive status is according to
|Species||Recently used synonym / misapplied name||Earliest record||Status in South Africa||Notes and references|
|Melaleuca alternifolia (Maiden & Betche) Cheel||1974||Introduced B2|
|Melaleuca armillaris subsp. armillaris||1930||Naturalized C3||Widely cultivated ornamental. Potentially invasive.|
|Melaleuca brachyandra (Lindl.) Craven||Callistemon brachyandrus Lindl.||1968||Introduced B2|
|Melaleuca bracteata F.Muell.||1981||Introduced B2|
|Melaleuca citrina (Curtis) Dum.Cours.||Callistemon citrinus (Curtis) Skeels||1932||Naturalized C3||
|Melaleuca cuticularis Labill.||1902||Introduced B2|
|Melaleuca decora (Salisb.) Britten||Melaleuca genistifolia Sm.||1963||Introduced B2|
|Melaleuca decussata R.Br.||1954||Introduced B2/B3|
|Melaleuca diosmifolia Andrews||1933||Introduced B2|
|Melaleuca elliptica Labill.||1963||Introduced B2||Observed in the deer park on the slopes of Devil’s Peak, Table Mountain, Cape Town. Possibly naturalized, but no supporting evidence.|
|Melaleuca flammea Craven||Callistemon acuminatus Cheel||1986||Introduced B2|
|Melaleuca fulgens R.Br.||1952||Introduced B2|
|Melaleuca huegelii subsp. huegelii||1945||Introduced B2|
|Melaleuca hypericifolia Sm.||1902||Invasive D2||
|Melaleuca incana subsp. incana||1967||Introduced B2|
|Melaleuca incana subsp. tenella (Benth.) Barlow||1981||Introduced B2|
|Melaleuca lanceolata Otto||1982||Introduced B2|
|Melaleuca lateritia A.Dietr.||1954||Introduced B2|
|Melaleuca linariifolia Sm.||1958||Introduced B2|
|Melaleuca linearis var. linearis||Callistemon linearis (Schrad. & J.C.Wendl.) Colvill ex Sweet, C. rigidus R.Br.||1902||Invasive D2||Several plants found at Kluitjieskraal and 56 plants (30–130 cm height range) were found at two sites in Grahamstown.|
|Melaleuca nesophila F.Muell.||1967||Introduced B2|
|Melaleuca nodosa Sm.||1961||Introduced B2|
|Melaleuca pachyphylla (Cheel) Craven||Callistemon pachyphyllus Cheel||1983||Introduced B2|
|Melaleuca paludicola Craven||Callistemon sieberi DC.||2011||Introduced B2|
|Melaleuca parvistaminea Byrnes||1933||Invasive E||Invading a wetland system,
|Melaleuca phoenicea (Lindl.) Craven||Callistemon phoeniceus Lindl.||1981||Introduced B2|
|Melaleuca quinquenervia (Cav.) S.T.Blake||Melaleuca leucadendra L.||1928||Naturalized C3||
|Melaleuca rhaphiophylla Schauer||1984||Introduced B2|
|Melaleuca rugulosa (Schltdl. ex Link) Craven||Callistemon rugulosus (Schltdl. ex Link) DC.||1961||Invasive D1/D2||Devil’s Peak, Cape Town. Spread > 500 m. ~20 adults. Seedlings growing in firebreak.|
|Melaleuca salicina Craven||Callistemon salignus (DC.) Colvill ex Sweet||1932||Naturalized C3|
|Melaleuca squarrosa Donn ex Sm.||1994||Introduced B2|
|Melaleuca styphelioides Sm.||1902||Naturalized C3||145 plants at Kluitjieskraal near the town Wosleley (60–450 cm height range)|
|Melaleuca subulata (Cheel) Craven||Callistemon subulatus Cheel||2013||Introduced B2/Naturalized C3||Near water body 10km NE of Villiersdorp, possibly at Rockview dam near Grabouw|
|Melaleuca teretifolia Endl.||1967||Introduced B2|
|Melaleuca thymifolia Sm.||1907||Introduced B2|
|Melaleuca viminalis subsp. viminalis||Callistemon viminalis subsp. viminalis||1948||Invasive D2||Widely planted with several localized sites of naturalization. Spreading along Kaaimans river ~3 km East of George|
List of Melaleuca species recorded in South Africa for which there is no confirmed herbarium record.
|Species||Earliest record||Source of information||Notes|
|Melaleuca hamulosa Turcz.||Unknown||
||No specimens found in PRE cultivated collection|
|Melaleuca glauca (Sweet) Craven [recorded as Callistemon speciosus (Sims) DC.]||Unknown||
||No specimens found in PRE cultivated collection|
|Melaleuca paludosa (Sweet) Craven [recorded as Callistemon glaucus (Bonpl.) Sweet]||1979||South African Plant Invaders Atlas (SAPIA)||Probably a misidentification. The only species found at the reported locality in Grahamstown is M. linearis.|
|Melaleuca pauperifolia F.Muell.||Unknown||
||No specimens found in PRE cultivated collection|
|Melaleuca wilsonii F.Muell.||1998||South African Plant Invaders Atlas (SAPIA, Australia’s Virtual Herbarium (MEL 2053098A)||Land owner at Honingklip near Botrivier in the Western Cape reports historic occurrence of “bottlebrushes” but no Melaleuca species occur at this site as of 2011.|
|Melaleuca nervosa (Lindl.) Cheel||Unknown||Gibbs (1998)||One tree recorded at Damara Farm near Malmesbury. Several Acacia species trials were also carried out at this site|
There are a number of ways that errors can be generated during the compilation of species lists (
Lists therefore require the application of taxonomic expertise on taxa not native to a particular region (
While genetic verification of species identifications is proving to be a reliable means of verifying a species, classical taxonomy still remains crucial to the identification of new species to a region (
Identification errors noted in this study have had direct implications. Melaleuca parvistaminea was initially misidentified in 2011 as the morphologically similar M. ericifolia. Melaleuca parvistaminea was only formally described in 1984 and collections prior to this were treated within the broad concept for M. ericifolia. Some M. armillaris subsp. armillaris specimens were also misidentified as M. ericifolia (e.g. NBG0269364). Melaleuca ericifolia is regarded as being predominantly clonal rather than reseeding. This affected management actions, through unforeseen profuse recruitment via seed after clearing and the absence of clonal spread and resprouting (
Effective pre-emptive control efforts rely heavily on whether alien species are listed as invasive in that region or are known to be invasive elsewhere (
Hybridization and horticultural selection for some Melaleuca species, especially those in the Callistemon group can further complicate accurate identification (
We identified ten species of Melaleuca naturalised in the Western Cape province of South Africa, but invasions of taxa in this genus are at an early stage, and there is likely to be a high level of invasion debt (sensu
We acknowledge financial support from the DST-NRF Centre of Excellence for Invasion Biology (C•I•B), Cape Nature, the South African National Department of Environment Affairs (DEA) through its funding of the South African National Biodiversity Institute’s Invasive Species Programme and through the collaborative research project “Integrated management of invasive alien species in South Africa” of the C•I•B and the DEA, and the National Research Foundation (grant 85417 to DMR). We are grateful to the many herbarium staff for their kind assistance, to Riki de Villiers for support with maps and to Pieter Winter for valuable comments on this manuscript.