A peer-reviewed open-access journal
PhytoKeys 172: 97–119 (2021)
Electronic identification keys for species with cryptic morphological characters
doi: 10.3897/phytokeys.172.53484
RESEARCH ARTICLE
http://phytokeys.pensoft.net
97
Launched to accelerate biodiversity research
Electronic identification keys for species with cryptic
morphological characters: a feasibility study using
some Thesium species
Natasha Lombard1,2, Margaretha Marianne le Roux1,2, Ben-Erik van Wyk2
1 Biosystematics Research and Biodiversity Collections Division, South African National Biodiversity Institute,
Private Bag X101, Pretoria, 0001, South Africa 2 Department of Botany and Plant Biotechnology, University
of Johannesburg, PO Box 524, Auckland Park, 2006, South Africa
Corresponding author: Natasha Lombard (n.lombard@sanbi.org.za)
Academic editor: M. A. Caraballo-Ortiz | Received 22 April 2020 | Accepted 24 August 2020 | Published 16 February 2021
Citation: Lombard N, le Roux MM, van Wyk B-E (2021) Electronic identification keys for species with cryptic
morphological characters: a feasibility study using some Thesium species. PhytoKeys 172: 97–119. https://doi.
org/10.3897/phytokeys.172.53484
Abstract
The popularity of electronic identification keys for species identification has increased with the rapid technological advancements of the 21st century. Although electronic identification keys have several advantages
over conventional textual identification keys and work well for charismatic species with large and clear morphological characters, they appear to be less feasible and less effective for species with cryptic morphology
(i.e. small, obscure, variable characters and/or complicated structures associated with terminology that is
difficult to interpret). This is largely due to the difficulty in presenting and illustrating cryptic morphological
characters unambiguously. When taking into account that enigmatic species with cryptic morphology are
often taxonomically problematic and therefore likely exacerbate the taxonomic impediment, it is clear that
species groups with cryptic morphology (and all the disciplines dependent on their correct identification)
could greatly benefit from a user-friendly identification tool, which clearly illustrates cryptic characters. To
this end, the aim of this study was to investigate and develop best practices for the unambiguous presentation of cryptic morphological characters using a pilot interactive photographic identification key for the
taxonomically difficult plant genus Thesium (Santalaceae), as well as to determine its feasibility. The project
consisted of three stages: (1) software platform selection, (2) key construction and (3) key evaluation. The
Copyright Natasha Lombard et al. 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.
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proposed identification key was produced with Xper3 software and can be accessed at http://www.xper3.fr/
xper3GeneratedFiles/publish/identification/1330098581747548637/mkey.html. Methodologies relating
to amongst others, character selection and delineation, visual and textual descriptions, key construction,
character coding and key evaluation are discussed in detail. Seventeen best practices identified during this
study are subsequently suggested for future electronic key compilation of species with cryptic morphology.
This study indicates that electronic identification keys can be feasible and effective aids for the identification
of species with cryptic morphological characters when the suggested best practices are followed.
Keywords
Best practice, interactive key, key construction, photographic key, Santalaceae, South African plants, taxonomic impediment, Xper3
Introduction
Species identification underpins the majority of biological sciences (Stevenson et al.
2003; Farr 2006; Farnsworth et al. 2013). Attributing a name to a specimen is central
to, amongst others, the classification of groups of organisms, ecology, species and habitat conservation, ecological restoration and the management of biological collections
(Lawrence and Hawthorne 2006; De Carvalho et al. 2007; Joly et al. 2014; Joly et al.
2019). Traditionally, textual dichotomous keys have been the main tools used for species identification (Walter and Winterton 2007; Nimis et al. 2012; Seo and Oh 2017).
More recently, rapid technological advancements of the 21st century have resulted in
the production of a wide array of electronic identification guides (Stevenson et al.
2003; Farnsworth et al. 2013) that range from simple textual electronic dichotomous
keys (e.g., Leistner 2000; Beuk 2019) to interactive mobile identification applications
(apps) with access to large multimedia databases (e.g., De Vaugelas et al. 2011; Merlin
Bird ID App, https://merlin.allaboutbirds.org/) and automatic visual recognition apps
(e.g., Zhao et al. 2015; PlantSnap, https://www.plantsnap.com/). Electronic identification keys have become commonplace (e.g., Kirchoff et al. 2011; Nimis et al. 2012; Seo
and Oh 2017; Jouveau et al. 2018; Bodin et al. 2019; Reeb and Gradstein 2020), are
relatively easy to produce and are aimed at enhancing the accessibility and usability of
identification keys, as well as the efficiency and accuracy of identifications (Drinkwater
2009; Kirchoff et al. 2011).
Although electronic identification keys have several advantages over conventional
identification keys [as detailed in Farr (2006) and Dallwitz et al. (2000)], the few
studies comparing the performance of these different identification keys have showed
mixed results. Stagg et al. (2015) showed that the accuracy and speed of woodland
moss identification was higher using a traditional dichotomous key than an electronic
key, while Seo and Oh (2017) found that orchid species were more accurately identified by senior college students when using an electronic identification key than when
using a textual dichotomous key or a guide book based on flower colour. Stagg and
Donkin (2017) showed that identifications of United Kingdom (UK) wild flowers
Electronic identification keys for species with cryptic morphological characters
99
were significantly more accurate using an electronic app than a guide book, but that
the identification accuracy of UK winter trees was significantly lower when using an
electronic app than when using guide books. Stagg and Donkin (2017) posited two
reasons for their contrasting results. First, the number of tree species was less than
the number of wild flowers so that browsing for tree species in the printed guides
was more time efficient than browsing for wild flowers of which there are many species (Drinkwater 2009; Stagg and Donkin 2017). Second, winter tree character states
were perceived as subjective, ambiguous and overall cryptic compared to wild flower
character states which were clear and concise (Stagg and Donkin 2017). These comparative studies indicate that while electronic identification keys such as interactive
photographic keys are effective when identifying charismatic species with large and
clear morphological characters, they are often ineffective when identifying enigmatic
species with cryptic morphological characters. Here cryptic characters (not to be confused with cryptic species) refer to any morphological character which might cause
uncertainty or confusion during the identification process due to one or a combination
of the following: (1) very small size [e.g., characteristics of leaf margins and venation
in mosses (Stagg et al. 2015); minute characters of armoured scale insects (Schneider
et al. 2019)], (2) obscure nature [e.g., subtle differences in bud colour of winter trees
(Stagg and Donkin 2017); metasternum related characters in some parasitoid wasps
(Klimmek and Baur 2018)], (3) intra-specific variation [e.g., flower colour variation in
the carnivorous plant genus Drosera L. (Drinkwater 2009); pronotum colour variation
in ladybirds (Jouveau et al. 2018)], and (4) complicated structures associated with terminology that is difficult to interpret [e.g., inflorescences of grasses (Fish et al. 2015);
thorax morphologies of Brazilian sand flies (Rocha et al. 2019)]. The challenge remains
to determine which aspects are critical to produce electronic identification keys that
can successfully identify species with cryptic morphological characters.
Enigmatic species with cryptic characters such as many plants, insects, bryophytes
and microorganisms are common and are often surrounded by much taxonomic uncertainty (Convention on Biological Diversity 2007). This is partly due to a research
bias towards charismatic species and partly due to the difficulty in finding and describing characters with which to delimit and identify enigmatic species. Often only one
or a few specialist taxonomists can accurately identify them. All of these aspects add
to the taxonomic impediment (Convention on Biological Diversity 2007; Walter and
Winterton 2007; Dar et al. 2012) and it is clear that species groups with cryptic characters (and all the disciplines dependent on their correct identification) could greatly
benefit from a user-friendly identification tool that clearly illustrates cryptic characters.
To address this need we investigated the use of a multi-access interactive photographic
identification key as an identification aid for selected species of the morphologically
difficult and near cosmopolitan genus Thesium L. [Santalaceae (The Angiosperm Phylogeny Group 2016)].
Thesium is a hemi-parasitic plant genus of ± 350 species that has its centre of diversity in southern Africa, with ± 175 species (Lombard et al. 2020). Some Thesium species are of economic importance (Lombard et al. 2020). For instance, T. humile Vahl
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has caused substantial losses to cereal crops in the Mediterranean region (Belakhdar et
al. 2014), while T. chinense Turcz. is sold commercially in Asia as an herbal medicine to
treat a wide array of ailments (Lombard et al. 2020). Species of this genus are notoriously difficult to identify due to, amongst others, the extreme intra-specific variation
observed in vegetative morphology, as well as their diminutive flowers (< 10 mm)
which contain several important diagnostic characters (Hill 1915). Identifications are
further complicated by the large number of species in the genus and the superficial
similarities among species (Hill 1915). Current identification keys for South African
Thesium species are textual keys (e.g., Hill 1925) that are often very difficult to use due
to the overlap of character states between couplets (to account for intra-specific variability), as well as the difficulty in describing subtle differences in the general impression, size and shape (GISS) of species (García et al. 2018). Thesium is therefore an ideal
group in which to study cryptic characters and their representation in an electronic
identification key.
The aim of this study was to investigate and develop best practices for the unambiguous presentation of cryptic morphological characters using a pilot interactive
photographic identification key. The project was developed by (1) identifying practical, easy-to-use software with which to construct a photographic identification key, (2)
producing a pilot identification key for 25 Thesium species found in the eastern part of
South Africa and (3) evaluating the effectiveness of the identification key with a target
group of users from different backgrounds. We subsequently propose a multi-access
interactive photographic identification key produced with Xper3 software.
Materials and methods
Taxa
As the intent of this study was to investigate and demonstrate principles behind the
unambiguous presentation of cryptic characters and not to produce a comprehensive
field-ready identification key, a subset of 25 species (Table 1) from the morphologically difficult genus Thesium were selected as a case study. These species are among ±
60 Thesium species that occur in the eastern part (summer rainfall area) of South Africa
and were chosen, firstly because they have been observed, collected and photographed
by the authors in their living state and natural habitat. Information and media collected in the field is advantageous when constructing photographic identification keys
and circumvents several problems associated with electronic key construction from
literature and preserved collections (see Morse et al. 1996; Drinkwater 2009). Second,
the majority of the 25 species are notoriously difficult to identify as is evidenced by
the numerous identification queries the authors received, as well as by the mixed specimen collections encountered in several South African herbaria. This indicates that even
trained taxonomists responsible for curating these collections had considerable difficulty in identifying the species in question. Third, recent (and ongoing) taxonomic stud-
Electronic identification keys for species with cryptic morphological characters
101
Table 1. The 25 Thesium species included in the pilot interactive photographic identification key, as well
as the most recent taxonomic treatment for each species.
Species
Thesium angulosum A.DC.
Thesium asterias A.W.Hill
Thesium confine Sond.
Thesium costatum A.W.Hill
Thesium cupressoides A.W.Hill
Thesium davidsoniae Brenan
Thesium durum Hillard & B.L.Burtt
Thesium goetzeanum Engl.
Thesium gracilarioides A.W.Hill
Thesium gracile A.W.Hill
Thesium gypsophiloides A.W.Hill
Thesium impeditum A.W.Hill
Thesium magalismontanum Sond.
Thesium multiramulosum Pilg.
Thesium natalense Sond.
Thesium ovatifolium N.Lombard & M.M.le Roux
Thesium pallidum A.DC.
Thesium procerum N.E.Br.
Thesium racemosum Bernh.
Thesium resedoides A.W.Hill
Thesium scirpioides A.W.Hill
Thesium transvaalense Schltr.
Thesium utile A.W.Hill
Thesium vahrmeijeri Brenan
Thesium zeyheri A.DC.
Taxonomic treatment used
Hill 1925
Hilliard 2006
Mashego and le Roux 2018
Hill 1925
Hill 1925
Brenan 1985
Mashego and le Roux 2018
Visser et al. 2018
Visser et al. 2018
Visser et al. 2018
Visser et al. 2018
Hill 1925
Hill 1925
Hilliard 2006
Lombard et al. in prep.
Lombard et al. 2019
Hill 1925
Visser et al. 2018
Hill 1925
Visser et al. 2018
Lombard et al. in prep.
Hill 1925
Hill 1925
Visser et al. 2018
Hill 1925
ies of 12 of the 25 species (Mashego and le Roux 2018; Visser et al. 2018; Lombard
et al. 2019, Lombard et al. in prep.) prompted the compilation of user-friendly identification keys and a platform for information dissemination to non-taxonomist users.
Fourth, the identification key contributes to research on Thesium that is considered a
high priority for taxonomic research in South Africa (Victor et al. 2015; Victor 2020).
Software platform: Xper3
Xper3 was chosen as the platform for the present study as it is a free access self-controlled programme where no external data storage or servers are needed, and which
includes all of the functionalities required by the authors (e.g., multi-access keys, visual
and text descriptors and species profiles) (Vignes-Lebbe et al. 2016; Vignes-Lebbe et
al. 2017; Pinel et al. 2017). The platform allows for remote access, is intuitive and
user friendly for both authors and users, allows for multiple contributors (including
concurrent data editing), has the option for both web-based and mobile interfaces and
can function as a taxonomic data management programme. The Xper3 home page can
be accessed at http://www.xper3.fr/ and detailed user documentation at http://wiki.
xper3.fr/lib/exe/fetch.php?media=wiki:xper3documentation.pdf.
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Key construction
Construction of the identification key was completed in four steps: 1) data collection,
2) taxonomic and character backbone construction, 3) character coding and 4) species
profile compilation.
Data collection
Characters and character states used
A total of 26 characters were used in the key (Table 2), including 24 discrete characters and two range characters. In the absence of a published or widely accepted list
of morphological characters for the genus, morphological characters and character
states were adapted from an unpublished character list by, and initial discussion
with, Daniel Nickrent (pers. comm.). All informative vegetative and reproductive characters that could clearly be shown with photographs were included. The
maximization of the number of morphological characters available to choose from
facilitates use by both non-specialist and specialist users. The majority of morphological characters included can be observed with the naked eye, but a 10x hand-lens
or light microscope is needed for some of the diminutive floral characters such as
style length, stigma position and placental column shape. Character states were
delineated and presented in such a way as to facilitate unambiguous interpretation
by users and following the guidelines provided in Walter and Winterton (2007);
also see Results and Discussion. Each of the provinces of South Africa were also included as characters in the key (see Table 2), as this proved to be the most efficient
and user-friendly way to account for the geographical distribution of each species.
Images
Live material was photographed in the field during the flowering seasons (September
to February) of 2016, 2017 and 2018 using a Canon EOS 400D camera and Canon
EF 100 mm/2.8 USM macro lens. Where live material could not be accessed for certain characters or species, photographs of herbarium material were used. One of the
advantages of electronic identification keys is that they can continuously be updated
and current images can be replaced with superior images as they become available.
Flowers from herbarium material were rehydrated by placing them in Windowlene
(cleaning agent) for 15 min before being photographed. Herbarium material were
photographed with standard smartphone cameras (Huawei P9 lite, Samsung S7) by
aiming the smartphone camera lens at the eyepiece of a light microscope (Nikon SMZ
745 T stereo microscope, Nikon Corporation) so that the enlarged image becomes
visible through the eyepiece and then taking the photo. Photographs were later ed-
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103
Table 2. The 26 characters and their respective character states used to distinguish between selected Thesium species in a pilot interactive photographic identification key. Definitions of characters and character
states are given in the identification key (http://www.xper3.fr/xper3GeneratedFiles/publish/identification/1330098581747548637/mkey.html).
Character
Distribution in
South Africa
(Province)
Habit 1 (shape)
Habit 2
(woodiness)
Habit 3
(branching
position)
Root system
1
Eastern Cape
2
Free State
3
Gauteng
Erect
Virgate
Decumbent or
procumbent
Woody
Herbaceous
Unbranched
From the
lower third
Branched
Underground
stem
Absent
Character state
4
5
KwaZulu-Natal Limpopo
From the
From the upper
middle third
third
Vegetative scales
Present
Plant height
(Actual measurement in m)
Stem crossSmooth
Ribbed
Winged (alate)
section
(sulcate)
Plant hairiness
Hairs absent Hairs present
(indumentum)
(glabrous)
(pubescent)
Foliage type
Leaves
Scales
Leaf orientation Appressed
Spreading Not applicable
Leaf attachment Fused to stem
Not fused
(decurrent)
to stem (not
decurrent)
Inflorescence
Indeterminate Determinate
1 - apex
Inflorescence
Raceme-like
Cymes
Spike-like
Solitary
2 - structure
Inflorescence 3 Monochasium Dichasium Not applicable
- synflorescence
flower
arrangement
combinations
Flower shape
Cup-shaped
Bell-shaped
Tubular
(stellate/
(campanulate)
patelliform)
Absent
Present
Involucral
bracts
Not fused
Partially fused Fully fused
Not applicable
Bract fusion
to flower
stalk (bract
recaulescence)
Bract shape
Lanceolate
Linear
Ovate
Deltoid
Corolla lobe
Triangular
Linear
shape
Flower disc
Present
Absent
Corolla
Dense hairs
Sparse hairs
Lacinulate Papillose (ciliate Smooth
lobe margin
or erose)
(glabrous)
hairiness
(indumentum)
Style length
Sessile
Short
Long
Stigma position
Below the
In line with
Above the
anthers
the anthers
anthers
Placental
Straight
Twisted
column shape
Fruit length
(Actual measurement in mm)
6
7
8
Mpumalanga Northwest Northern
Cape
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ited where necessary to enhance characters using Microsoft PowerPoint software v.
14.0.7229.5000 (Microsoft Corporation). All photographs included here and in the
key were taken by the authors unless stated otherwise. Bract shape and placental column shape photographs were supplemented with illustrations to ensure unambiguity
(Leggett and Kirchoff 2011).
Taxonomic and character backbone construction
Taxonomic backbone
The first data to be uploaded into Xper3 were the scientific names of the 25 Thesium
species included in this study (Fig. 1; Table 1). Sound taxonomy is a crucial prerequisite for identification key construction. Therefore, species concepts and names
were taken from the most recent taxonomic treatments of each species, which are
provided in Table 1.
Figure 1. Xper3 author interface showing A the list of 25 Thesium species (items) which forms the
taxonomic backbone of the interactive photographic identification key, as well as B an example of the
supplementary information provided for T. angulosum.
Electronic identification keys for species with cryptic morphological characters
105
Character backbone
After the taxonomic backbone was completed the character backbone was compiled.
This was done by adding each character and its corresponding character states into
Xper3. Each character and character state was listed in the key using descriptive terms
such as flower shape, style length etc. (e.g., Fig. 2). Generalist terminology was sometimes used and specialist terminology added in brackets where applicable to cater for
specialist users. Where needed, terminology was supplemented with textual descriptions further explaining what was being shown (e.g., Fig. 2).
In addition to terminology and textual descriptions, each character and character
state was also visually represented with a figure plate containing representative photographs. For example, the character vegetative scales, was illustrated with three photographs; two plants with vegetative scales and one without vegetative scales (Fig. 3).
Where possible, each character state was illustrated with multiple photographs to enhance clarity. For example, the branched character state of the root system character
was illustrated with three photographs and the underground stem character state with
six photographs (Fig. 4). Due to the small and cryptic nature of many morphologi-
Figure 2. The Xper3 author interface showing A the list of 26 characters (descriptors) which forms the
character backbone of the interactive photographic identification key, as well as B an example of the supplementary information provided for the character, style length.
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Figure 3. An example of the visual and textual presentation of a character, vegetative scales, in the user
interface of the interactive photographic identification key. A representative images of each character state
(present and absent) of the character, with the relevant structures further emphasized using circles and
arrows B a textual description of the character.
Figure 4. An example of the visual and textual presentation of character states in the user interface
of the interactive photographic identification key. For the character, root system, each character state
(branched and underground stem) is A illustrated with multiple photographs to show variation, as well
as B a textual description.
cal structures, relevant characters and/or character states were highlighted in certain
images, either by a circle or an arrow. Individual images were labelled where needed for clarity. All figure plates were compiled in Microsoft PowerPoint software v.
14.0.7229.5000 (Microsoft Corporation), exported as JPEG files, resized to a standard
height of 1000 pixels using FastStone Photo Resizer 3.8 software (FastStone Soft),
saved to Dropbox and uploaded into Xper3 by copying the Dropbox link for each
figure plate to the “Add from Url” feature in Xper3. All photographs and figures were
compiled based on the best practices provided by Leggett and Kirchoff (2011).
Character coding
After constructing the taxonomic- and character backbones of the key, character states
were manually coded for each species in Xper3, for example, the style length of T. angulosum is long (Fig. 5). The appropriate character states for each species were determined
by the authors through examining species in the field, as well as studying herbarium material at the National Herbarium in Pretoria (PRE), South Africa. Subsequent
Electronic identification keys for species with cryptic morphological characters
107
Figure 5. The Xper3 author interface showing an example of character state coding in the interactive
photographic identification key, where the style length of Thesium angulosum is coded as long.
knowledge gaps were filled using the most recent taxonomic description available for
each species (Table 1). It was occasionally necessary to select more than one character
state for a species to account for the intra-specific variation observed in Thesium species, as well as differences in user interpretation (see Results and Discussion). Character
weighting was not utilized in this study.
Species profiles
The final step in key construction was to create a profile for each species (Fig. 6) that
includes contextual photographs, a detailed distribution map, a short diagnosis and
a list of character states for that species (automatically generated by Xper3). Photographs included here show important diagnostic characters, as well as other general
impressions of each species (e.g., the habit and flowers) to aid identification. The short
diagnoses give notes on separating morphologically similar species. Where needed,
comparisons with similar species not presented in the key were also included to ensure
correct identifications despite the nature (pilot study) of the key.
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Figure 6. An example of a species profile with supplementary information in the user interface of the
interactive photographic identification key, showing A representative photographs, B a distribution map,
C diagnostic notes and D a list of character states of Thesium gracile.
Key evaluation
Target group testing
A target group testing was done at a Plant Specialist Group meeting at Buffelskloof Nature Reserve, South Africa. The 22 participants included amateur botanists, conservationists, ecologists, environmental consultants, horticulturists and taxonomists. Partici-
Electronic identification keys for species with cryptic morphological characters
109
pants were divided into six groups of three or four and provided with access to the Xper3
key on their smartphones and laptops, a printed dichotomous key (automated by the
Xper3 platform), a microscope and a flower dissecting kit (a razor blade, tweezers and
dissecting needle). Each group was given ample fresh material of three Thesium species
(T. confine Sond., T. procerum N.E.Br. and T. utile A.W.Hill) and was asked to identify
them accurately at their own pace. During the exercise participants provided feedback
which allowed characters, character states, terminology and photographs that caused
confusion and/or uncertainty to be identified. Participants also gave general feedback
on the usability of the key and all of these suggestions were incorporated into an improved key (discussed below). The authors aim to continuously improve the key by trial
and revision and also expand the key by systematically adding more Thesium species.
Checkbase
In addition to the target group testing, the identification key was also evaluated using
Checkbase, a build-in tool provided by Xper3. Checkbase provides information on discrimination between (1) items (species), (2) descriptions (characters) and (3) character
states, as well as (4) missing character states.
Results and discussion
In the current age of information and digital technology more emphasis is being
placed on the development of electronic resources to advance the identification of
species, which is vital for all practices related to or dependent on biological studies
(Walter and Winterton 2007; Kirchoff et al. 2011). One of the remaining challenges in
electronic identification key development, namely the effective presentation of cryptic
morphological characters to ensure successful identifications in morphologically
difficult species groups, was addressed in a pilot study using a Thesium identification
key. The identification key is accessible through the following link: http://www.xper3.
fr/xper3GeneratedFiles/publish/identification/1330098581747548637/mkey.html.
Software platform selection
While Xper3 software provided a pragmatic platform for key construction in this
study, the general principles and best practices discussed hereafter, can be applied to
any software with the relevant functionalities (e.g., DELTA, http://www.delta-intkey.
com/; Lucid, http://www.lucidcentral.org/). Walter and Winterton (2007), Drinkwater (2009) and Dallwitz et al. (2000) amongst others provide summaries of the general
advantages of interactive keys, which are applicable to all electronic keys but not the
specific focus of this study.
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Multi-access keys
Software platforms with a multi-access approach, where a user can choose any of the
available characters throughout the key, circumvent multiple problems associated with
the identification of species, especially those with cryptic characters (Walter and Winterton 2007; Drinkwater 2009). Compared to single-access keys, where characters follow
on each other in a predetermined order, multi-access keys allow users to select the characters that are available and that they are most confident about, thereby optimizing identification accuracy (Morse et al. 1996; Drinkwater 2009). It also decreases the chances
of a user abandoning the identification process altogether due to the cryptic nature of
some characters (e.g., a minute ovary that can only be accessed by dissecting a flower)
or guessing character states, which might lead to misidentifications (Morse et al. 1996).
Multi-access keys furthermore cater for the unambiguous presentation of cryptic
characters and character states by allowing authors to utilize numerous character divisions. For example, the inflorescence structure of Thesium species is an important
distinguishing character, but often varies considerably and is notoriously difficult to
interpret. Its incorporation into traditional textual keys (Hill 1915, 1925) has resulted
in several overlapping character states between divisions, the use of vague phrases such
as “more or less” and other complex terminology. When taking into account that inflorescence type is only the second division in Hill’s key, it is understandable that users
have struggled to identify Thesium species correctly. In contrast, the electronic key
proposed here clearly delineates different inflorescence types using three characters and
nine character states with no overlap and also illustrates each division with both visual
(including multiple photographs) and text aids.
Updatable keys
Software allowing for updates and changes to be made to identification keys after publication is pertinent for species groups with cryptic morphology as these groups are
likely to be taxonomically problematic and subject to ongoing taxonomic study. For
example, subsequent to the construction of the identification key presented here, a Thesium species new to science was described (Lombard et al. 2019) and a taxonomic revision of two species in the key completed (Lombard et al. in prep.). Information from
both these studies was easily incorporated into the database in Xper3. The addition of
new species to electronic keys is especially important in enigmatic species groups with
cryptic characters as the electronic key might be one of the only user-friendly information sources available to non-specialist users. Furthermore, minimizing the lag time
between taxonomic research and its availability to the end user, for example through
an identification key, might contribute somewhat to alleviating the taxonomic impediment (Walter and Winterton 2007). In addition to research, user feedback and
its incorporation is central to a study like the one presented here as user experience is
the ultimate measure of both the success of cryptic character presentation and species
identifications, and allows for continual improvement of the identification key.
Electronic identification keys for species with cryptic morphological characters
111
Species profiles
Species profiles with supplementary information and media on each species form part
of many software platforms and contribute considerably to accurate identifications
(Kumar et al. 2012). Xper3 species’ profiles include, amongst others, contextual photographs, detailed distribution maps and short diagnoses, and can easily be accessed at
any point in the identification process. In dealing with species with cryptic morphology, it is recommended that users follow the key until they are uncertain about all of
the remaining characters. If more than one species remains, the profiles of the remaining species should be consulted for a final identification (one can flip from one profile
to the next in Xper3) (Drinkwater 2009). Detailed distribution maps are also very
useful as they are unambiguous and instantly allow a user to determine whether the
species in question occurs in the applicable geographical area. Furthermore, the value
of contextual photographs displaying the general impression, size and shape (GISS) of
a species should not be overlooked. While two species might differ in only one or two
particularly cryptic characters, they are often easily distinguishable by their GISS. “A
picture is worth a thousand words” and relays information which is difficult to capture
in words. For species with cryptic morphology, photographs are the crux of resolving
confusion originating from traditional textual identification keys. Lastly, the short diagnosis provided for each species further streamlines the identification process by providing information on similar species and how they differ from one another (Stevenson
et al. 2003). Species profiles can also be used independently of the identification key to
confirm species identities or for additional information on a particular species.
Key construction
Character and character state delineation
In this study, maximizing the number of valuable characters while minimizing the number of associated character states proved most pragmatic. Contrary to species groups
with clearly defined morphological characters (e.g., Jouveau et al. 2018), maximizing
the number character options in morphologically difficult groups provides more opportunities for users to select characters that they are certain about (Walter and Winterton 2007; Drinkwater 2009). One caveat of this approach is that it is time consuming to work through many characters (Stagg et al. 2015). However, algorithms giving
continual preference to characters with the most discriminatory power, as is the case in
Xper3, offsets this limitation to some degree (Walter and Winterton 2007; Drinkwater
2009). Furthermore, in challenging species groups, increased identification accuracy
should arguably take preference over identification time. In the case of Thesium specifically, identification time using the interactive photographic key is unlikely to exceed
identification time using the traditional textual keys provided by Hill (1915, 1925).
The electronic key further improves identification efficiency by subdividing particularly confusing and cryptic characters into more digestible units (Drinkwater
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2009). During the reconstruction and revision of the identification key, this approach
not only resulted in a more user-friendly key but also allowed for more precise character coding (Drinkwater 2009). For instance, the habit (growth form) of Thesium
species, although often variable (Cohn 2004; Luo et al. 2012; Gamoun 2014), is an
important distinguishing character. To improve the unambiguity of this valuable character, habit was divided into three separate characters namely, shape, woodiness and
branching position. Furthermore, minimizing the number of character states that users
are presented with at each character facilitated ease of use and decreased the chances of
incorrect user interpretation.
Character and character state presentation
One of the main advantages of electronic identification keys when identifying species
with cryptic characters is the illustration of characters using multiple aids, which greatly reduces ambiguity (Lawrence and Hawthorne 2006; Drinkwater 2009; De Vaugelas
et al. 2011). Optimal visual presentation of each character and character state ideally
requires sufficient photographs to illustrate the full range of variation, thereby leaving
little to no room for user misinterpretation (see Kirchoff et al. 2011). For species with
cryptic morphology, electronic key construction therefore goes hand in hand with
field observations and photographs of live material. Unfortunately, in the majority of
cases, acquiring the necessary photographs remains a major challenge due to resource
and logistical constraints, especially in groups with many or rare species. Nevertheless,
without adequate visual aids, the efficient and accurate identification of species with
cryptic characters is improbable.
It is also true that images may contain only partial information (Joly et al. 2019)
and should thus be supplemented with textual aids that are tailored to the requirements of the target audience. In the case of Thesium (and likely other species groups
with cryptic morphology) the need for a user-friendly identification guide that can be
used by both specialist and non-specialist users was immediately apparent. While generalist terminology saves non-specialist users the time and resources needed to familiarize themselves with the workings of a specific group, specialist terminology allows
specialists to cross-reference information in the key with other taxonomic literature.
Key evaluation
Checkbase
The Xper3 evaluation tool Checkbase showed that five species pairs were only partially
discriminated: (1) T. racemosum Bernh. and T. costatum A.W.Hill, (2) T. gracilarioides
A.W.Hill and T. multiramulosum Pilg., (3) T. gracilarioides A.W.Hill and T. resedoides
A.W.Hill, (4) T. gracile A.W.Hill and T. utile A.W.Hill, and (5) T. asterias A.W.Hill and
T. ovatifolium N.Lombard & M.M.le Roux. These species pairs are morphologically
Electronic identification keys for species with cryptic morphological characters
113
similar and the coding of multiple character states to account for variation resulted in
partial, but not full, overlap in some characters. While this result highlights the challenge of successfully separating species with cryptic morphology using electronic keys
(as well as traditional keys), these species can nonetheless be successfully identified using their respective species profiles as discussed before. All of the characters and character states included in the key provided full discrimination between species (as opposed
to only partial discrimination or no discrimination). One exception was the Western
Cape Province character state under the geographical distribution character, as none of
the species included in the key occur in the province. It was, however, retained along
with the other eight provinces of South Africa for completeness and to allow for future
expansion in the scope of the key.
Target group evaluation
The target group evaluation indicated that the proposed key could be useful for identifying species with cryptic morphological characters and provided valuable suggestions
for improvement that were subsequently incorporated. Differences in user interpretation of character states had to be addressed and subsequently, following Kirchoff et
al. (2011) and Leggett and Kirchoff (2011), some arrows and/or circles were added.
Furthermore, we replaced images causing uncertainty with superior images and incorporated labels.
During the evaluation, it was clear that some characters were problematic. Participants had very subjective interpretations of the degree of woodiness of plants
(originally divided into herbs, suffrutices and shrubs) and consequently had trouble
identifying the correct character state. To address this unambiguity, the number of
character states was reduced to two: plants that were obviously herbaceous (including
suffrutices) and robust woody plants. Corresponding textual descriptions were also
revised and expanded, and clearer photographs were used to illustrate each character
state. Similarly, the difficult-to-interpret inflorescence structure was simplified from six
complex character states (e.g., monotelic racemose inflorescence with a terminal dichasial cyme, and simple or compound dichasial and monochasial cymes) to four, more
general types (raceme-like, spike-like, cymes and solitary). The majority of participants
were not able to utilize the placental column shape (generally < 2 mm) as they could
not successfully dissect flowers to access this structure. Although there is little that can
be done to improve this hurdle, the character was retained in the key as it is valuable
for specialist use, and it is not crucial for species identification so that non-specialist
users can simply forgo it.
The last method employed to improve the accuracy of the identification key was
the coding of multiple character states (multiple correct answers) where necessary. This
step is crucial as it accounts for intra-specific variation in characters, characters with
continuous character states and also for user subjectivity (Drinkwater 2009; Stagg et
al. 2015). For example, participants had difficulty determining the character state for
corolla lobe hairs, partly due to user subjectivity and partly due to the fact that there
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is an almost continuous range of character states, from dense hairs to sparse hairs
to papilla to smooth lobes. It is suggested that multiple character states are coded
where a character state of a species is intermediate between two character states in the
key, thereby resolving the problem of continuous characters, as well as subjective user
interpretation. This flexibility in coding optimizes the chances of correct identifications without jeopardizing the discriminatory power of the key, as species are separated
based on a combination of many characters. However, this approach should be applied
conservatively to ensure that overall distinguishing power is not significantly reduced
and that characters do not become redundant (see Jouveau et al. 2018). In Xper3, the
key can easily be checked for redundancies using the item ‘comparison tool’, which
indicates whether each character provides full discrimination, partial discrimination or
no discrimination between species.
Suggested best practices
Based on the pilot electronic identification key presented here, the following best
practices are suggested for the unambiguous presentation of cryptic morphological
characters and their character states in electronic identification keys: (1) maximization
of the number of valuable characters; (2) minimization of the number of character
states associated with each character; (3) division of difficult/complex characters into
multiple simpler characters; (4) illustration of characters and character states using
multiple aids such as visual and text descriptions; (5) illustration of character states
using multiple photographs to show the entire range of variation (if applicable); (6)
use of photographs of live material (as opposed to preserved material) and plants in
situ where possible; (7) addition of labels and accents such as arrows or circles to photographs to highlight relevant characters; (8) tailoring text descriptions to the target
audience(s) (generalist or specialist terminology, or both); and (9) coding for multiple
character states (multiple correct answers) where intra-specific variation is present or if
a species falls on or close to the border between two character states (to ensure that the
discriminatory power of characters is not lost).
Other general best practices include: (10) ensuring sound taxonomy and clearly
defined species concepts prior to key construction; (11) using software that allows for
updates and improvements (as necessitated by user feedback and ongoing research),
including the replacement of images with superior ones as they become available;
(12) utilizing a multi-access key approach [as opposed to a single-access approach (dichotomous or polychotomous)]; (13) using species profiles with representative photographs and supplementary information including (14) photographs of diagnostic
features and the general impression, size and shape (GISS); (15) detailed distribution
maps (if species are geographically separated) and (16) diagnostic notes separating
morphologically similar species; and (17) evaluation of proposed identification keys
by participants from the target audience and the subsequent incorporation of feedback prior to publication.
Electronic identification keys for species with cryptic morphological characters
115
Conclusions
Electronic identification keys are valuable resources for species identification, which
underpins all biological sciences. This study contributes to the rather limited body
of knowledge on the successful identification of enigmatic species with cryptic morphologies using contemporary identification aids. It has shown that well-constructed
electronic identification keys are feasible and offer the possibility of accurate identifications, in particular for species with cryptic characters, despite apparent contradictory
reports in the literature. We have gained valuable insights into not only the problems
and challenges associated with the successful identification of Thesium species (as a
practical example of species groups with cryptic morphology) but also possible solutions and circumventions for difficulties in electronic key construction.
Ultimately a sound knowledge of the taxonomy and diagnostic characters of the
taxa will determine the quality and efficacy of the identification key, regardless of the
technology used in its construction and presentation. High attention to the presentation of the characters and their respective states are critical. There is no substitute
for careful field studies of live organisms in their natural environment to overcome
the typical limitations imposed by preserved specimens. This means a much greater
effort in data collection but also a much greater reward in achieving a high level of
discriminatory power in the identification key. Such electronic identification keys
maximise the benefits that can be derived from the use of digital images and undoubtedly increase the accuracy of identification and reduce ambiguities that lead to a more
user-friendly product for both specialist and generalist users. This might be especially
valuable in economically important species groups such as grasses, which are characterised by cryptic morphological characters, by expanding the suit of potential users to
farmers, conservationists, ecologists and so forth. The gap between research and users
can also be minimised by adding the latest information on subjects such as synonyms,
ecology and potential uses to species profiles.
To our knowledge, the best practices suggested here (although a combination of
novel and previously known guidelines) are the first guidelines on electronic identification key construction tailored to species with cryptic morphology. While these
guidelines work well for Thesium, similar studies of other species groups with cryptic
morphologies will test these best practices, and likely reveal additional challenges and
guidelines. This study therefore serves as a starting point for similar studies.
Acknowledgements
The following persons and institutions are thanked: the Botanical Education Trust, Foundational Biodiversity Information Programme (Small Grant number 104931), University
of Johannesburg, South African National Biodiversity Institute (SANBI) and National
Research Foundation of South Africa (Grant number 84442) for funding; the National
Herbarium under the SANBI for hosting the study and access to their collections; Andrew
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Hankey, Barbara Turpin, Bronwynn Egan, Daniel Nickrent, Delia Oosthuizen, Kate and
Graham Grieve, John Burrows, Kagiso Mashego and Sedzani Simali for assistance in the
field; persons from the Plant Specialist Group and Buffelskloof Nature Reserve for hosting
and participating in the evaluation of the identification key; Sylvain Bouquin for technical
assistance with the Xper3 platform; Daniel Nickrent from Southern Illinois University for
his contribution to an initial version of the identification key, and advice on morphological terminology, characters and character states; two reviewers, Lynn Bohs and Muthama
Muasya, for suggesting improvements to the identification key and manuscript.
References
Belakhdar G, Benjouad A, Kessabi M, Abdennebi EH (2014) Identification of the pyrrolizidine
alkaloid 1-hydroxymethylpyrrolizidine from Thesium humile Vahl. Journal of Materials and
Environmental Science 5(3): 811–814.
Beuk P (2019) Key: Scatopsidae. https://www.online-keys.net/infusions/keys/keys_view.
php?key_no=23 [accessed 30.03.2020]
Bodin SC, Scheel-Ybert R, Beauchêne J, Molino J-F, Bremond L (2019) CharKey: An electronic identification key for wood charcoals of French Guiana. IAWA Journal 40(1): 75–91.
https://doi.org/10.1163/22941932-40190227
Cohn J (2004) Effects of slashing and burning on Thesium australe R. Brown (Santalaceae) in coastal grasslands of NSW. Proceedings of the Linnean Society of New South Wales 125: 57–65.
Convention on Biological Diversity (2007) What is the problem? The taxonomic impediment.
https://www.cbd.int/gti/problem.shtml [accessed 19.12.2019]
Dallwitz MJ, Paine TA, Zurcher EJ (2000) Principles of interactive keys. https://www.deltaintkey.com/www/interactivekeys.pdf [accessed 26.09.2018]
Dar GH, Khuroo AA, Reddy CS, Malik AH (2012) Impediment to taxonomy and its impact
on biodiversity science: An Indian perspective. Proceedings of the National Academy of
Sciences. India. Section B, Biological Sciences 82(2): 235–240. https://doi.org/10.1007/
s40011-012-0031-3
De Carvalho MR, Bockmann FA, Amorim DS, Brandão CRF, de Vivo M, de Figueiredo JL,
Britski HA, de Pinna MCC, Menezes NA, Marques FPL, Papavero N, Cancello EM, Crisci JV, McEachran JD, Schelly RC, Lundberg JG, Gill AC, Britz R, Wheeler QD, Stiassny
MLJ, Parenti LR, Page LM, Wheeler WC, Faivovich J, Vari RP, Grande L, Humphries
CJ, DeSalle R, Ebach MC, Nelson GJ (2007) Taxonomic Impediment or impediment to
taxonomy? A commentary on systematics and the Cybertaxonomic-Automation Paradigm.
Evolutionary Biology 34(3–4): 140–143. https://doi.org/10.1007/s11692-007-9011-6
De Vaugelas J, Leyendecker V, Leca H, Luc P, Noel P, Riva J-C, Sabatier A, Souty-Grosset
C (2011) Use of smartphones (iPhoneTM, AndroidTM, etc.) for the field identification of
European crayfish. Knowledge and Management of Aquatic Ecosystems 401(34): 1–6.
https://doi.org/10.1051/kmae/2011063
Drinkwater RE (2009) Insights into the development of online plant identification keys based
on literature review: An exemplar electronic key to Australian Drosera. Bioscience Horizons
2(1): 90–96. https://doi.org/10.1093/biohorizons/hzp007
Electronic identification keys for species with cryptic morphological characters
117
Farnsworth EJ, Chu M, Kress WJ, Neill AK, Best JH, Pickering J, Stevenson RD, Courtney
GW, Van Dyk JK, Ellison AM (2013) Next-generation field guides. Bioscience 63(11):
891–899. https://doi.org/10.1525/bio.2013.63.11.8
Farr DF (2006) On-line keys: More than just paper on the web. Taxon 55(3): 589–596. https://
doi.org/10.2307/25065636
Fish L, Mashau AC, Moeaha MJ, Nembudani MT (2015) Identification guide to southern African grasses. An identification manual with keys, descriptions and distributions. Strelitzia 36. South African National Biodiversity Institute, Pretoria, 1–798.
https://archive.org/details/identificationgu36lfis
Gamoun M (2014) Grazing intensity effects on the vegetation in desert rangelands of southern
Tunisia. Journal of Arid Land 6(3): 324–333. https://doi.org/10.1007/s40333-013-0202-y
García MA, Nickrent DL, Mucina L (2018) Thesium nautimontanum, a new species of Thesiaceae (Santalales) from South Africa. PhytoKeys 109: 41–51. https://doi.org/10.3897/
phytokeys.109.28607
Hill AW (1915) The genus Thesium in South Africa, with a key and descriptions of new species.
Bulletin of Miscellaneous Information, Kew 1: 1–43. https://doi.org/10.2307/4115447
Hill AW (1925) Order CXX. Santalaceae. In: Thiselton-Dyer WT (Ed.) Flora Capensis. L.
Reeve & Co. LTD., London, 135–212. https://doi.org/10.2307/4107506
Joly A, Goëau H, Bonnet P, Bakić V, Barbe J, Selmi S, Yahiaoui I, Carré J, Mouysset E,
Molino J-F, Boujemaa N, Barthélémy D (2014) Interactive plant identification based
on social image data. Ecological Informatics 23: 22–34. https://doi.org/10.1016/j.ecoinf.2013.07.006
Joly A, Goëau H, Botella C, Kahl S, Servajean M, Glotin H, Bonnet P, Planqué R, RobertStöter F, Vellinga W-P, Müller H (2019) Overview of LifeCLEF 2019: identification of
amazonian plants, South & North American birds, and niche prediction. In: Crestani F,
Braschler M, Savoy J, Rauber A, Müller H, Losada DE, Bürki GH, Cappellato L, Ferro N
(Eds) Experimental IR meets multilinguality, multimodality, and interaction. CLEF 2019.
Lecture Notes in Computer Science, volume 11696. Springer, Cham, 387–401. https://
doi.org/10.1007/978-3-030-28577-7_29
Jouveau S, Delaunay M, Vignes-Lebbe R, Nattier R (2018) A multi-access identification key
based on colour patterns in ladybirds (Coleoptera, Coccinellidae). ZooKeys 758: 55–73.
https://doi.org/10.3897/zookeys.758.22171
Kirchoff BK, Leggett R, Her V, Moua C, Morrison J, Poole C (2011) Principles of visual key
construction – with a visual identification key to the Fagaceae of the southeastern United
States. AoB Plants plr005: 1–48. https://doi.org/10.1093/aobpla/plr005
Klimmek F, Baur H (2018) An interactive key to Central European species of the Pteromalus
albipennis species group and other species of the genus (Hymenoptera: Chalcidoidea: Pteromalidae), with the description of a new species. Biodiversity Data Journal 6: e27722.
https://doi.org/10.3897/BDJ.6.e27722
Kumar N, Belhumeur PN, Biswas A, Jacobs DW, Kress WJ, Lopez I, Soares JVB (2012) Leafsnap: a computer vision system for automatic plant species identification. In: Fitzgibbon
A, Lazebnik S, Perona P, Sato Y, Schmid C (Eds) Computer Vision – ECCV 2012. ECCV
2012. Lecture Notes in Computer Science, volume 7573. Springer, Berlin, Heidelberg,
502–516. https://doi.org/10.1007/978-3-642-33709-3_36
118
Natasha Lombard et al. / PhytoKeys 172: 97–119 (2021)
Lawrence A, Hawthorne W (2006) Plant identification: creating user-friendly field guides for
biodiversity management. Earthscan, London, 1–275. https://books.google.co.za/books?
id=CNFuyOVTSf4C&printsec=frontcover&source=gbs_ge_summary_r&cad=0#v=onep
age&q&f=false
Leggett R, Kirchoff BK (2011) Image use in field guides and identification keys: review and
recommendations. AoB Plants plr004: 1–37. https://doi.org/10.1093/aobpla/plr004
Leistner OA (Ed.) (2000) Seed plants of southern Africa: families and genera. Strelitzia 10.
National Botanical Institute, Pretoria. http://biodiversityadvisor.sanbi.org/wp-content/
themes/bst/keys/e-Key-20160604/Index.html [accessed 08.10.2018]
Lombard N, le Roux MM, Van Wyk B-E (2019) Thesium ovatifolium (Santalaceae), a new
species with ovate leaves from KwaZulu-Natal, South Africa. Phytotaxa 405(5): 263–268.
https://doi.org/10.11646/phytotaxa.405.5.5
Lombard N, van Wyk B-E, le Roux MM (2020) A review of the ethnobotany, contemporary
uses, chemistry and pharmacology of the genus Thesium (Santalaceae). Journal of Ethnopharmacology 256: 112745. https://doi.org/10.1016/j.jep.2020.112745
Luo F, Guo Q, Wang C, Zhang X (2012) Complex evaluation for influence of hosts on hemiparasite Thesium chinense. Zhongguo Zhongyao Zazhi 37: 1174–1179.
Mashego KS, le Roux MM (2018) A taxonomic evaluation of the Thesium confine species complex (Santalaceae). Bothalia 48(1): a2346. https://doi.org/10.4102/abc.v48i1.2346
Morse DR, Tardivel GM, Spicer J (1996) A comparison of the effectiveness of a dichotomous
key and a multi-access key to woodlice. https://kar.kent.ac.uk/21343/1/WoodliceMorse.pdf
Nimis PL, Riccamboni R, Martellos S (2012) Identification keys on mobile devices: The Dryades experience. Plant Biosystems 146(4): 783–788. https://doi.org/10.1080/11263504.
2012.740089
Pinel A, Bouquin S, Bourdon E, Kerner A, Vignes-Lebbe R (2017) Three years of Xper3 assessment: Towards sharing semantic taxonomic content of identification keys. Proceedings of
TDWG 1: e20382. https://doi.org/10.3897/tdwgproceedings.1.20382
Reeb C, Gradstein R (2020) A taxonomic revision of Aneuraceae (Marchantiophyta) from
eastern Africa with an interactive identification key. Cryptogamie. Bryologie 41(2): 11–34.
https://doi.org/10.5252/cryptogamie-bryologie2020v41a2
Rocha D, Almeida M, Batista J, Andrade A (2019) LutzoDex™ – A digital key for Brazilian
sand flies (Diptera, Phlebotominae) within an Android App. Zootaxa 4688(3): 382–388.
https://doi.org/10.11646/zootaxa.4688.3.4
Schneider SA, Fizdale MA, Normark BB (2019) An online interactive identification key to
common pest species of Aspidiotini (Hemiptera, Coccomorpha, Diaspididae), version 1.0.
ZooKeys 867: 87–96. https://doi.org/10.3897/zookeys.867.34937
Seo S-W, Oh S-H (2017) A visual identification key to Orchidaceae of Korea. Korean Journal
of Plant Taxonomy 47(2): 124–131. https://doi.org/10.11110/kjpt.2017.47.2.124
Stagg BC, Donkin ME (2017) Apps for angiosperms: The usability of mobile computers and
printed field guides for UK wild flower and winter tree identification. Journal of Biological
Education 51(2): 123–135. https://doi.org/10.1080/00219266.2016.1177572
Stagg BC, Donkin ME, Smith AM (2015) Bryophytes for beginners: The usability of a printed
dichotomous key versus a multi-access computer-based key for bryophyte identification.
Electronic identification keys for species with cryptic morphological characters
119
Journal of Biological Education 49(3): 274–287. https://doi.org/10.1080/00219266.201
4.934900
Stevenson RD, Haber WA, Morris RA (2003) Electronic field guides and user communities
in the eco-informatics revolution. Conservation Ecology 7(1): 3. https://doi.org/10.5751/
ES-00505-070103
The Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group
classification for the orders and families of flowering plants: APG IV. Journal of the Linnean Society 181(1): 1–20. https://doi.org/10.1111/boj.12385
Victor JE (2020) Research strategy for plant taxonomy 2020–2030. South African National
Biodiversity Institute. https://www.sanbi.org/wp-content/uploads/2020/03/Researchstrategy-for-plant-taxonomy-2020-2030.pdf [accessed 18.04.2020]
Victor JE, Smith GF, Van Wyk A (2015) Strategy for plant taxonomic research in South Africa
2015–2020. SANBI Biodiversity Series 26. South African National Biodiversity Institute,
Pretoria, 1–39. https://www.sanbi.org/wp-content/uploads/2018/04/biodiversity-series26-strategy-plant-taxonomic-research-sa.pdf
Vignes-Lebbe R, Chesselet P, Diep Thi MH (2016) Xper3: nouveaux outils pour le travail collaboratif, la formation et la transmission des connaissances sur les phénotypes végétaux. In:
Rakotoarisoa NR, Blackmore S, Riera B (Eds) Botanists of the twenty-first century. Roles,
challenges and opportunities. United Nations Educational, Scientific and Cultural Organisation, Paris, 228–239. https://unesdoc.unesco.org/ark:/48223/pf0000243791
Vignes-Lebbe R, Bouquin S, Kerner A, Bourdon E (2017) Desktop or remote knowledge base
management systems for taxonomic data and identification keys: Xper2 and Xper3. Proceedings of TDWG 1: e19911. https://doi.org/10.3897/tdwgproceedings.1.19911
Visser N, le Roux MM, van Wyk B-E (2018) A taxonomic revision of the Thesium goetzeanum
species complex (Santalaceae) from Lesotho, South Africa and Swaziland. South African
Journal of Botany 119: 45–62. https://doi.org/10.1016/j.sajb.2018.08.005
Walter DE, Winterton S (2007) Keys and the crisis in taxonomy: Extinction or reinvention? Annual Review of Entomology 52(1): 193–208. https://doi.org/10.1146/annurev.
ento.51.110104.151054
Zhao Z-Q, Ma L-H, Cheung Y-M, Wu X, Tang Y, Chen CLP (2015) ApLeaf: An efficient
android-based plant leaf identification system. Neurocomputing 151: 1112–1119. https://
doi.org/10.1016/j.neucom.2014.02.077