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Insect Systematics and Diversity, 1(1), 2017, 3–19 doi: 10.1093/isd/ixx004 Taxonomy Forum
New Species Described From Photographs: Yes? No? Sometimes? A Fierce Debate and a New Declaration of the ICZN
Frank-Thorsten Krell,1,3 and Stephen A. Marshall2
1Department of Zoology, Denver Museum of Nature & Science, 2001 Colorado Blvd, Denver, CO 80205-5798, 2Department of Environmental Biology, University of Guelph, Guelph, ON H1G 2W1, Canada, and 3Corresponding author, e-mail: frank.krell@dmns. org
Subject Editor: István Mikó
Received 25 May 2017; Editorial decision 17 August 2017
Abstract The option of describing new taxa using photographs as proxies for lost or escaped (‘unpreserved’) type specimens has been rarely used but is now undergoing renewed scrutiny as taxonomists are increasingly equipped to capture descriptive information prior to capturing and preserving type specimens. We here provide a historical perspective on this practice from both nomenclatural and practical points of view, culminating in a summary and discussion of a new Declaration of the International Commission of Zoological Nomenclature containing recommendations about descriptions without preserved specimens. We conclude that although descriptions using photographs as proxy types are Code-compliant and occasionally justified, the conditions under which such descriptions are justified are likely to remain relatively rare. Increasing restrictions on specimen collecting, which we deplore because of the centrality of collecting and collections to all of biodiversity science, could lead to more ‘proxy type’ descriptions in those taxa in which photographs can provide sufficient information for descriptions, but we predict that such cases will remain infrequent exceptions.
Key words: nomenclature, photograph, proxy type, taxonomy
Most of us were taught in our academic infancy that the descrip- and is becoming increasingly repetitive but demonstrates that the tion of a new species requires a published description and a desig- issue is a controversial one. The coincidence of the launch of Insect nated type, and most entomologists involved with the discovery and Systematics and Diversity and the publication of a Declaration by description of new species realize that many other criteria should be the International Commission on Zoological Nomenclature (ICZN) met in order to justify a species description. We do not all agree on in March 2017 on descriptions without preserved types (ICZN exactly where the bar should be set, but there is general agreement 2017) led to the drafting of this paper. Our aim is to calm the waves that new species must at a minimum be justified in the context of by giving a historical perspective of the issue, clarifying the rules of related and similar species and must be diagnosable. Descriptions of nomenclature, and emphasizing the centrality of taxonomic judg- species that cannot be subsequently recognized are detrimental, and ment and good practice. descriptions of species outside the context of the rest of their clade are usually of little use. The requirements for a published description The Rules: What Does the Zoological and a designated type are embedded in the International Code of Zoological Nomenclature (ICZN 1999) and are governed by spe- Code Say? cific rules; the criteria for justified species descriptions and ‘good’ The International Code of Zoological Nomenclature (‘the Code’, taxonomy are matters of taxonomic judgement. ICZN 1999) is a set of rules and guidelines designed to ensure that While new species have occasionally been described and for- the names used to communicate about biodiversity are unique, uni- mally named without a preserved type specimen, a recent paper by versal, and stable. The requirements that must be met to add a for- Marshall and Evenhuis (2015) explicitly discussing and executing mal species name to the language of science are, critically, governed such a procedure sparked a heated worldwide debate on social media by explicit rules that all taxonomists must abide by, whether or not and in a still growing number of formal publications. This discus- their new descriptions meet the subjective criteria of good science. sion has sometimes drifted into emotional or uninformed arguments And one of the best known of those requirements is that all new
© The Author 2017. Published by Oxford University Press on behalf of Entomological Society of America. 3 All rights reserved. For Permissions, please email: [email protected]. Copyedited by: OUP
4 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
species names must be linked to an individual or voucher that serves the description, if any (Code Art. 72.4.1). If he had none, then only as the objective standard for the species name. Normally that indi- the specimens from the references count for the type series. Article vidual will be a preserved specimen such as a pinned insect or slide 72.4.1 allows for this not uncommon situation and is explained fur- mount, but the Code does allow for exceptions such as the loss or ther by Art. 72.5.6: ‘In the case of a nominal species-group taxon destruction of the type specimen before or after description. The loss based on an illustration or description, or on a bibliographic refer- of types after description is common. For example, the original types ence to an illustration or description, the name-bearing type is the of over 10% of all snake species are missing or lost (Wallach and specimen or specimens illustrated or described (and not the illustra- Jones 1994) and ca. 30–40% of all accepted nemertean names lack tion or description itself).’ Article 73.1.4. says essentially the same a preserved type specimen (Crandall et al. 2001). The Code recog- thing in a different context. nizes that such secondarily typeless species only occasionally cause When all the species from previous literature were classified in the problems and provides for the resolution of problems that do arise Linnaean binominal style, new species descriptions became almost through the designation of replacement types (neotypes). The loss exclusively linked to preserved specimens, except for groups in which of types prior to the publication of a description is less common, specimen preservation poses a problem, such as protists (Duszynski and is the issue at hand. Despite claims to the contrary (e.g., Landry 1999, Aescht 2008, Lainson et al. 2008, Lahr et al. 2012), ctenophores 2005, Timm et al. 2005, Santos et al. 2016, Garraffoni and Freitas (Matsumoto 1988), or meiofaunal slugs (of which at least the extracted 2017), the Code explicitly allows the naming of a species after the DNA could serve as the holotype with the rest of the specimen being type is lost or destroyed, as explained below. The description of a destroyed in the extraction process; Jörger and Schödl 2013). In such new species using a photograph as a proxy for a lost type is thus in groups, species descriptions without preserved type material have compliance with the Code. always been common, unavoidably so. A binding rule requiring pre- Some of the participants in the proxy type debate object to this served type specimens would exclude those branches of zoology from provision in the Code, describing it as a loophole, complaining that the zoological Code. But what about ‘preservable’ taxa, such as insects it was written before the modern era of digital photography, and and vertebrates? Here too, there is a history of descriptions without calling for it to be changed. It is important to understand that a preserved material, but it is a much shorter one (Table 1). change in the Code to disallow the use of photographs as proxies for lost types would not change the underlying taxonomy. The processes Type Specimens Not Preserved at Time of of discovery and description of species, which are matters of taxo- Description nomic judgment rather than rules, would remain the same. But if the There are numerous historical examples of species described without Code were changed to disallow descriptions based on lost types then original specimens having been directly studied. One such example new species represented only by photographic (or other) records is Billberg’s ichthyological paper from 1833, in which he described of unpreserved specimens would have to be named or referred to three new species of pipefish (now all junior synonyms) from draw- under a system independent of the Code and would thus lack uni- ings that the soldier and artist Johan Wilhelm Palmstruch had made versality and stability. Alternatively, such new discoveries could be 30 yr before from living animals (Kullander 2016). This is as close as left without any sort of name, unnecessarily hampering communi- it gets to photo-based descriptions in times when photography was cation and clarity. The nomenclatural aspect of this controversy is yet to be invented, but such descriptions of species by authors with- thus just about whether and what name to apply to a species, not out first-hand knowledge of the type specimens are now explicitly an issue of the reality, legitimacy, or value of a species discovery and discouraged by the Code: ‘An author should designate as holotype description. Scientific quality is not governed by the Code. One of a specimen actually studied by him or her, not a specimen known to the explicit underlying principles upon which the Code is based—in the author only from descriptions or illustrations in the literature.’ fact the first principle listed in the introduction to the Code—is that (ICZN 1999, Recommend. 73B). it ‘refrains from infringing on taxonomic judgement, which must not While photo-based descriptions of preservable taxa have be made subject to regulation or restraint’. Taxonomic judgement is appeared in the scientific literature more frequently since the advent an important issue, and criteria for distinguishing ‘good’ taxonomy of accessible digital photography, such examples are still extremely from ‘bad’ taxonomy are of fundamental interest to every taxono- rare (Table 1) compared with the 17–20,000 new species described mist, editor, and reviewer. But these criteria vary widely from taxon every year (IISE 2011). Such descriptions without preserved type to taxon and from case to case. In most circumstances, the choice specimens are a continuum (Table 1) including: to describe a taxon on the basis of a lost or seriously damaged type specimen would stand out as poor taxonomic judgement, but under - taxa described from living, captured specimens that mostly some exceptional circumstances it is justified and cases of ‘typeless’ were later preserved (Delacour and Labouille 1924, Nicolai descriptions (good and bad!) have periodically appeared for decades. 1972, Brown 1987, Meier et al. 1987, Böhme and Ziegler 1997, We here present a short history of these cases before going on to Zimmermann et al. 1997, Tomey 2000, Kappeler et al. 2005, examine the more recent controversy over ‘proxy types’. Andriantompohavana et al. 2006); - photographed specimen with parts preserved (e.g., feathers, blood, A Short History of Descriptions Based on or tissue samples) (Smith et al. 1991; Olsen et al. 2002; Thalmann and Geissmann 2005; Athreya 2006; Andriantompohavana et al. Illustrations or Without Preserved Type 2006, 2007; Louis et al. 2006, 2008; Zaramody et al. 2006; Material Olivieri et al. 2007; Lei et al. 2008, 2015; Radespiel et al. 2008, The naming and description of species based on previously published 2012; Gentile and Snell 2009; Barrera et al. 2010; Frasier et al. illustrations was a common practice in the early time of Linnaean 2016; Hotaling et al. 2016; Andriaholinirina et al. 2017; Craul taxonomy. When Linnaeus compiled his Systema Naturae, he listed et al. 2017); all known species whether he had seen specimens or not. His type - studied and preserved specimen that got lost between description series consist of all the specimens depicted or described in the cited and publication of the description (Dyne and Jamieson 2004, references, plus specimens he had in his collection at the time of Kieneke et al. 2015); Copyedited by: OUP
Insect Systematics and Diversity, 2017, Vol. 1, No. 1 5
Table 1. Species of preservable taxa, described in the 20th and 21st centuries without preserved name-bearing whole-body type specimen at the time of description, in chronological order. Bold: species the authors of which did not intend or were unable to preserve physical types (specimens or parts). The examples of this group are likely to be complete. The examples of types consisting of minor physical parts, such as fur, DNA, or blood samples, are comprehensive but certainly not complete
Taxon Types History Current status
Leptoplana mediterranea Bock Described from draw- Conditionally described as form of Valid (Gammoudi et al. 2012). 1913 (Platyhelminthes: ings published by Lang Leptoplana tremellaris from the figures by Polycladida: Leptoplanidae) (1884). Lang (1884). Nomenclatural availability confirmed and elevated to species level by Gammoudi et al. (2012) who misstated the type locality though. Lophura imperialis Delacour Types specimen ‘in Coll. The female syntype was preserved in the Identified as a hybrid (Hennache and Jabouille 1924 (Aves: J. Delacour’, later speci- Muséum National d’Histoire Naturelle in et al. 2003). Galliformes: Phasianidae) fied as alive ‘in my aviary Paris upon its death in 1927 and was avail- at Clères’ (Delacour and able for morphological and genetic studies; Jabouille 1925). the male syntype was lost during World War II (Hennache et al. 2003). Hypochera lorenzi Nicolai Holotype specimen alive, Synonymized by Payne (1976) with H. wil- Synonymized (Elzen 2010). 1972 (Aves: Passeriformes: in the institute’s posses- soni which seems to be more variable than Viduidae) sion, later preserved in a Nicolas considered. The type was preserved museum collection (Elzen in the Bonn museum by 1982 or earlier 2010). (Payne 1982). Hoplolatilus geo Fricke Photographs, no pre- Described from photographs and observa- Valid (Earle and Pyle 1997). and Kacher 1982 (Pisces: served parts; no types tions with a submersible at 80–116 m Perciformes: Malacanthidae) designated depth. Collection of specimens impossible. Malurus campbelli Schodde Holotype designated from Specimens were netted, photographed, and Valid (Driskell et al. 2011). and Weatherly 1983 (Aves: photograph, drawing banded but not collected. Later a speci- Passeriformes: Maluridae) from photograph pub- men could be preserved (Schodde 1984). lished, archival prints of Currently in the genus Chenorhamphus photographs deposited in Oustalet (Driksell et al. 2011). museum collections. Pytilia melba flavicaudata Holotype designated from Described in a self-published work on the Status currently unclear (color Welch et al. 1986 (Aves: photograph; no pre- basis of a photograph of the holotype and variant or subspecies) (Payne Passeriformes: Estrildidae) served parts. Photograph two paratypes; photographs deposited in 2010). in museum collection, the Natural History Museum London. not published. Redescribed by Welch and Welch (1988), still as ‘subsp. nov.’. Here the authors con- sider the three additional males mentioned in the original descriptions as paratypes, photos of which are in the same museum collection. Payne (1989) suggests to con- sider the subspecies ‘invalid until specimens have been collected’ which is not supported by the Code. Later, Welch and Welch (1992) note that ‘The taxonomic status of the birds in Djibouti remains unclear.’ Hapalemur aureus Meier et al. Holotype captured, photo- No explicit reason for not preserving the hol- Valid (Wright and Tan 2016). 1987 (Mammalia: Primates: graphed, measured, cata- otype is given, but it was regarded as highly Lemuridae) logued, and kept alive endangered. Current status of the holotype in captivity in a zoo. unknown to us. Fausser et al. (2002) stud- Karyotype described. ied five specimens from the zoo where the Intent to deposit the holotype was kept but did not mention that holotype specimen after specimen. death in collection. Parosphromenus allani Brown Living specimens. Preliminary description from living aquarium Valid (Kottelat and Ng 2005). 1987 and Parasphromenus Photographs pub- specimens; intended full description was harveyi Brown 1987 (Pisces: lished, but ‘Neither of never published. Type depository not pub- Perciformes: Osphronemidae) the specimens in these lished. As the type material of both species photographs are the was preserved, it could be revised and lec- holotypes for the new totypes designated (Kottelat and Ng 2005). species.’ Besides saying what is not the holotype, the author did not clarify which specimens are the holotypes. Type mate- rial now preserved in a museum collection. Copyedited by: OUP
6 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
Table 1. Continued
Taxon Types History Current status
Lonchura spectabilis sepik- Holotype designated from Payne (2010: 376) ‘provisionally included’ Unresolved. ensis Jonkers and Roersma photograph, photograph it in (= synonymized it with) another 1990 (Aves: Passeriformes: deposited in museum. No subspecies. Estrildidae) preserved parts. Laniarius liberatus Smith et al. Holotype designated, This is the first case of a bird holotype sin- Synonymized (Nguembock et al. 1991 (Aves: Passeriformes: photographed, specimen gleton that was deliberately released (after 2008). Malaconotidae) released. Preserved parts: description, after a year in captivity, and DNA, three drops of dry 175 km from its place of capture) which blood on a piece of paper caused wide discussion and criticism (see (kept deep frozen), two Collar 1999). The preserved blood samples tubes of blood (in EDTA allowed reassessment of the species within buffer), and moulted a molecular phylogenetic analysis of the feathers mounted on a genus Laniarius, resulting in the synonymi- cardboard zation of L. liberatus with L. erlangeri (Nguembock et al. 2008). Cryptophidion annamense Three color slides taken in The detailed description provided Pauwels Unresolved. Wallach and Jones 1994 1968. Holotype desig- and Meirte (1996) with the opportunity (Squamata: Serpentes) nated from photographs. for a detailed critique, resulting in the No preserved parts. synonymization of the species. This was strongly rebutted by the authors (Wallach and Jones 1996) and one of the referees of the paper (Lazell 1996). Treated as valid genus in the family Colubridae by Zaher et al. (2009) and as a valid species by Das (2015), but, e.g., Wogan et al. (2012) accepted Pauwels and Meirte’s syononymy. Varanus melinus Böhme and Living, catalogued speci- Four specimens were imported from Obi Valid (Böhme 2014). Ziegler 1997 (Squamata: mens. Photographs pub- Island, Indonesia, to Germany. One of Varanidae) lished. Holotype and one them was obtained for the vivarium of the paratype now preserved Museum Koenig in Bonn and designated as in a museum collection. the holotype. The paratypes were promised to the same Museum after their death, but only one of them ended up preserved in the Bonn collection (Böhme 2014). Böhme now considers it a mistake having used living specimens as types that are in the posses- sion of other people and not guaranteed to be preserved in the designated repository (Böhme 2014). Microcebus ravelobensis Holotype and paratype The species was described by Zimmermann Valid (Yoder et al. 2016). Zimmermann et al. 1997 were living, catalogued et al. (1998), but is actually available (Mammalia: Primates: specimens, maintained at from a previously published abstract Cheirogaleidae) a zoo and intended for (Zimmermann et al. 1997). While holo- and preservation in a public paratype were intended for preservation in collection. a public collection, they were not preserved after they died and are lost (Rasoloarison et al. 2000). No preserved parts of the type series are documented. Rasoloarison et al. (2000) designated a preserved specimen as the neotype. Bebearia banksi Hecq and Holotype designated from Re-interpreted and synonymized by the junior Synonymized (Larsen 2005). Larsen 1998 (Insecta: videotape, of which pho- author seven years later (Larsen 2005). Lepidoptera: Nymphalidae) tographs are published. No physical evidence preserved. Badis badis bengalensis Tomey Living specimens, types ‘Animals in the type series live under my Synonymized (Kullander and 2000 (Pisces: Perciformes: designated on published care. I intend to deposit them after death Britz 2002). Badidae) photographs. Types in NNM, Leiden’. This had not yet hap- intended to be preserved pened when the family Badidae was revised in a museum collection. and the subspecies synonymized 2 yr later (Kullander and Britz 2002), but the inten- tion of the author to deposit type specimens according to Art. 16.4.2. was clearly stated, making the name available. Copyedited by: OUP
Insect Systematics and Diversity, 2017, Vol. 1, No. 1 7
Table 1. Continued
Taxon Types History Current status
Ninox sumbaensis Olsen et al. Holotype ‘was collected A reason why the body was not preserved Valid (Madika et al. 2011, 2002 (Aves: Strigiformes: [shot] by a local bird for science was not given. According to Peterson 2014). Strigidae) hunter. The body was left Peterson (2014) ‘the specimen documenta- with villagers on Sumba. tion of its phenotype is only very fragmen- Feathers and photo- tary, so comparisons with other, similar graphs are lodged [and taxa will forever be difficult.’ However, in properly accessioned] at the original description the cytochrome b Heidelberg University’. gene was sequenced, obtained from the col- lected feathers, and the sequence compared to that of related species. Diplotrema glareaphila Holotype and paratypes Based on an unpublished description and Valid. Dyne and Jamieson, 2004 designated and repre- illustrations by the senior author. The types (Annelida: Oligochaeta: sented by drawings. got lost before publication of the descrip- Acanthodrilidae) Lodgement of types tion. According to the Earthworm Species unknown at time of database (see Csuzdi 2012) the name description. is unavailable, not complying with Art. 16.4 (ICZN 1999). This is incorrect since holotype and paratypes were designated, but were, for all intents and purposes, no longer extant so that Art. 16.4.2 (intent to deposit) does not apply. Lophocebus kipunji Ehardt Holotype and paratype ‘The number of individuals in each of the two Valid (Davenport et al. 2016). et al. in Jones et al. 2005 designated from pho- populations of this species is undoubtedly (Mammalia: Primates: tographs, no preserved very small; no live individual shouls be col- Cercopithecidae) parts. lected at this time to serve as the holotype. The Rungwe-Livingstone pupulation is des- ignated the source population for physical specimens in support of the holotype.’ (Jones et al. 2005). When a specimen became avail- able for study a year after the description, the species was transferred into its own, new genus, Rungwecebus Davenport et al. 2006, and a variety of research initiated. Macaca munzala Sinha et al. Holotype and paratypes No specimen preserved because of ethical Unresolved (Biswas et al. 2011), 2005 (Mammalia: Primates: designated from pho- considerations. The authors intended to col- but considered valid by Sinha Cercopithecidae) tographs, No preserved lect paratypes post-description and deposit (2016). parts. them in collections. However, paratypes cannot be designated after the description is published. In the year of the published description, a specimen became available, killed by local people in self-defence, which was then described in detail and correctly called a ‘voucher specimen’ (Mishra and Sinha 2008). Biswas et al. (2011) did not consider M. munzala a distinct species but could not resolve its taxonomic status. Microcebus lehilahytsara Roos Six syntypes alive at zoo, No intention for deposition of deceased type Valid (Yoder et al. 2016). and Kappeler in Kappeler DNA preserved, meas- specimens stated. Fate of the specimens et al. 2005 (Mammalia: ured, photographed. unknown to us. Primates: Cheirogaleidae) Avahi cleesei Thalmann and Holotype captured, photo- The species is considered endangered. The Valid (Thalmann and Baden Geissmann 2005 (Mammalia: graphed, videographed, authors did not collect a specimen for ethi- 2016), but questioned by Primates: Indriidae) audiotaped, and released. cal reasons. Zaramody et al. (2006). Hair samples preserved in museum collection. Cebus queirozi Mendes Pontes Holotype and paratype Simultaneously, de Oliveira and Langguth Synonymized (Rylands and and Malta in Mendes Pontes designated. Holotype (2006) re-establish Simia flava Schreber, 1774, Mittermeier 2009). et al. 2006 (Mammalia: captured, measured and and designate a neotype. In a note added in Primates: Cebidae) photographed, then proof, they state the identity of C. queirozi released without preser- with Schreber’s species, but explicitly do not vation of parts. Paratype declare it a junior synonym because they photographed. erroneously consider C. queirozi unavailable as it is described without a preserved type specimen. Rylands and Mittermeier (2009) finally synonymize the two names. Copyedited by: OUP
8 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
Table 1. Continued
Taxon Types History Current status
Liocichla bugunorum Athreya Holotype captured, photo- According to Peterson (2014) ‘Conversations Valid (Peterson 2014). 2006 (Aves: Passeriformes: graphed, measured, and with the author of the description indicate Leiothrichidae) released. Some feathers that no specimen was collected because deposited in museum government regulations made collection of collection. a more complete specimen impossible at the time.’ Lepilemur ahmansoni, Syntypes captured, pho- ‘Due to the inability to maintain sportive Valid (Wilmet et al. 2014). Lepilemur fleuretae, tographed, measured, lemurs as long-term live vouchers in captiv- Lepilemur grewcocki, blood samples taken and ity, the type series [...] are represented by Lepilemur hubbardi, preserved, and specimens whole blood samples from free-ranging Lepilemur jamesi, released. Two syntypes of individuals along with a database contain- Lepilemur milanoii, L. milanoii held alive in ing all field data, accessioned sequence Lepilemur seali, a zoo, microchip tagged data, and photographs’ (Louis et al. 2006). Lepilemur tymerlachsoni, and ear biopsies sampled. Since photos and data cannot be part of Lepilemur wrighti Louis et al. a type series, the type series consist of 2006 (Mammalia: Primates: the specimen pictured in these photo- Lepilemuridae) graphs and physically represented by the blood samples. – Hoffmann et al. (2009) emended L. ahmansoni to L. ahmansono- rum, L. grewcocki to L. grewcockorum, L. hubbardi to L. hubbardorum, L. jamesi to L. jamesorum, L. tymerlachsoni to L. tymerlachsonorum, and L. wrighti to L. wrightae because of grammatically wrong endings according to the stated dedi- cations. However, Article 32.5.1. (ICZN 1999) states that incorrect latinization must not be corrected, and the original spellings be maintained. Microcebus mamiratra Holotype captured, pho- Current status of the holotype unknown to Valid (Louis and Lei 2016, Yoder Andriantompohavana et al. tographed, measured, us. et al. 2016). 2006 (Mammalia: Primates: microchip tagged, and Cheirogaleidae) kept alive in captivity in a zoo. Tissue samples preserved. Microcebus mittermeieri, Holotypes alive in zoo, Current status of the holotypes unknown to Valid (Yoder et al. 2016). Microcebus jollyae, microchip tagged. Ear us. Microcebus simmonsi Louis biopsies and blood et al. 2006 (Mammalis: preserved. Primates: Cheirogaleidae) Avahi peyrierasi, Avahi meridi- Holotypes captured, meas- No explicit reason for not preserving the full Valid; A. ramanantsoavani con- onalis, Avahi meridionalis ured, skin biopsies taken holotype is given. sidered distinct species (Louis ramanantsoavani Zaramody and preserved, specimens 2016d). et al. 2006 (Mammalia: released. Primates: Indriidae) Avahi betsileo Holotype captured, pho- No explicit reason for not preserving the Valid (Louis 2016a). Andriantompohavana et al. tographed, measured, full holotype is given, but ‘the highly 2007 (Mammalia: Primates: blood sample taken and folivorous dietary requirements of this Indriidae) preserved, and specimen group of lemurs currently precludes released. Total genomic any attempts to curate “live vouchers”’ DNA for three paratypes (Andriantomopohavana et al. 2007). preserved. Microcebus bongolaven- Holotypes captured, pho- No full specimens were preserved because the M. bongolavensis and M. dan- sis, Microcebus danfossi, tographed, measured, novelty of the species was only discovered fossi valid; M. lokobensis syn- Microcebus lokobensis Olivieri ear biopsies and hair later in the lab. Very late in the production onymized (Yoder et al. 2016). et al. 2007 (Mammalia: samples taken, specimens of the paper, specimens were preserved of Primates: Cheirogaleidae) released. each of the new species and included as paratypes while it was too late to use them as the holotypes (U. Radespiel, pers. comm., 2017). Facilitated by preserved genetic material, M. lokobensis was synonymized with M. mamiratra Andriantompohavana et al., 2006 as a consequence of parallel descriptions (Louis et al. 2008). Copyedited by: OUP
Insect Systematics and Diversity, 2017, Vol. 1, No. 1 9
Table 1. Continued
Taxon Types History Current status
Dulichiella terminos Lowry Holotype designated and Ledoyer’s (1986) detailed description Valid (Paz-Ríos and Adrisson and Springthorpe 2007 species described from and illustrations allowed Lowry and 2014). (Crustacea: Amphipida: figures in Ledoyer (1986) Springthorpe (2007) to include and Melitidae) who had misidentified describe the species as new in their revision the species as D. appen- of the genus. diculata; ‘whereabouts of specimen not known, probably no longer extant’. Avahi mooreorum, Lepilemur Syntypes captured, pho- No explicit reason for not preserving the full Valid (Louis 2016b,c). scottorum Lei et al. 2008 tographed, measured, holotype is given, but ‘the highly folivorous (Mammalia: Primates: blood sample taken and dietary requirements of these groups of Indriidae and Lepilemuridae) preserved, microchip lemurs currently precludes any attempts to tagged, and specimen curate “live vouchers”’ (Lei et al. 2008). released. Microcebus margotmarshae, Holotypes captured, meas- No explicit reason for not preserving com- Valid (Yoder et al. 2016). Microcebus arnholdi Louis ured, ear biopsies and plete holotypes is given, but the threatened et al. 2008 (Mammalia: blood samples taken, status of lemurs was mentioned in the Primates: Cheirogaleidae) microchip tagged, introduction. According to the descriptions, specimens released. Total photos exist for the paratypes, but were not genomic DNA preserved. mentioned for the holotypes. The webpage for the Appendix with more detailed infor- mation was inaccessible [29 July 2017]. Microcebus macarthurii Holotype captured, photo- 'The animal itself was released [...] since its Valid (Yoder et al. 2016). Radespiel et al. 2008 graphed, measured, ear taxonomic distinctiveness was not recog- (Mammalia: Primates: biopsies and hair samples nized at the time of capture' (U. Radespiel, Cheirogaleidae) taken, and specimen pers.comm. 2017). released. Conolophus marthae Gentile Holotype captured, The species was discovered in 1986 and Valid (Onorati et al. 2017). and Snell 2009 (Squamata: branded, transpondered, identified as distinct and studied in depth Iguanidae) photographed, measured, by Tzika et al. (2008) and Gentile et al. and released. Blood sam- (2009). It was informally named ‘rosada’ ple preserved in museum before it was finally named in a Code- collection. Intent to compliant way by Gentile and Snell deposit the holotype (2009). Despite preserved physical evidence specimen after death in (blood), the release of the holotype has collection. drawn harsh criticism (Nemésio 2009) but was equally strongly defended by Donegan (2009). Frick (2010) explains that the measures taken by the authors to relocate the specimen after its death do not guaran- tee that the specimen can be found. Grallaria fenwickorum Barrera Specimen captured, pho- Peterson (2013, 2014) considered the pre- Valid. and Bartels in Barrera et al. tographed, and released. served feathers undiagnostic. The species 2010 (Aves: Passeriformes: Some feathers were was described simultaneously, but pub- Grallariidae) preserved. Two preserved lished slightly later, by Carantón-Ayala and complete specimens Certuche-Cubillos (2010), the discoverer of were photographed in the new species, with the preserved speci- the description, but not mens as types. This story is full of politics, designated types because paperwork issues, problematic behaviour, they were collected lack- financial incentives, rivalry, etc. (Regalado ing a relevant permit. 2011, Fundación ProAves de Colombia 2013) and as a whole does not reflect well on the taxonomic and conservation com- munity. Peterson (2013) applied to the ICZN to designate one of the preserved specimens as the neotype and Fundación ProAves (2013) added alternative propos- als. The results of the ICZN’s vote are yet to be published. Forpus flavicollis Bertagnolio 31 syntypes designated on a Donegan et al. (2011) considered the syntypes Synoymized (Donegan et al. and Racheli 2010 (Aves: photograph (of the inter- dyed specimens of a parrotlet common in 2011). Psittaciformes: Psittacidae) net). No preserved parts. the area and synonymized the species. Copyedited by: OUP
10 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
Table 1. Continued
Taxon Types History Current status
Microcebus gerpi Radespiel et al. Holotype captured, meas- ‘The animal itself was released [...] since its Valid (Yoder et al. 2016). 2012 (Mammalia: Primates: ured, photographed, hair taxonomic distinctiveness was not recog- Cheirogaleidae) and tissue samples taken, nized at the time of capture’ (Radespiel and specimen released. et al. 2012). Strix omanensis Robb et al. Holotype designated Robb et al. (2013) discovered that Strix Synonymized. 2013 (Aves: Strigiformes: from photo. No parts butleri comprised two species, compared Strigidae) preserved. that battered type of this species with the photographs of a specimen from Oman and decided that the latter is a new spe- cies. Kirwan et al (2015), also studying the S. butleri type, assumed the synonymy with S. omanensis, which was confirmed by Robb et al. (2016) when they had captured a specimen and could study DNA. Macaca leucogenys Li et al. Holotype and two para- Li et al. (2015) state that ‘Due to ethical con- Valid (Fan et al. 2017). 2015 (Mammalia: Primates: types designated from cerns regarding killing wild primates, we Cercopithecidae) camera trap pho- did not obtain a voucher specimen for the tographs. No parts proposed new species’. In the year of the preserved. description, skins of the species from speci- mens killed by local dogs became available and are now preserved in a museum col- lection (Fan et al. 2017), and soon after a ‘specimen’ was collected for studying the mitochondrial genome (Hou et al. 2016). Marleyimyia xylocopae Holotype captured after This paper triggered the most extensive Valid. Marshall and Evenhuis seven photographs by the discussion on the topic of photo-based 2015 (Insecta: Diptera: senior author but later description so far. Bombyliidae) escaped. Paratype had previously escaped after eight photographs, prior to capture. Presbytis johnaspinalli Nardelli Holotype and ‘ten syntypes’ Nijman (2015) claimed that the specimens Unresolved. 2015 (Mammalia: Primates: (=paratypes) designated are ‘most likely’ bleached specimens of Cercopithecidae) from five photographs a known langur species. Nardelli (2016) ‘from the internet and questions Nijman’s reasoning and defends publications’. the status of a distinct species. Cephalodasys interinsula- Holotype studied alive, Two specimens were studied alive (one fully Valid. ris Kieneke et al. 2015 photographed and meas- mature, one subadult) and a third specimen (Gastrotricha: Macrodasyida: ured, no longer extant. was studied after fixation and was partially Cephalodasyidae) Paratype preserved. damaged. ‘Since only a single mature speci- men was studied alive, this specimen is des- ignated as the holotype even though it is no longer extant. [...] The specimen prepared for SEM [...] is designated as a paratype specimen’ and preserved in a museum. Cheirogaleus andysabini Lei Holotype captured, meas- No explicit reason for not preserving the Valid (Rowe 2016). et al. 2015 (Mammalia: ured, ear biopsies and complete holotype is given, but preva- Primates: Cheirogaleidae) blood samples taken, lent habitat destruction in the area and microchip tagged unknown conservation status of the species is mentioned elsewhere in the paper. Nothybus absens Lonsdale Holotype escaped after Valid. and Marshall 2016 (Insecta: photograph by the sec- Diptera: Nothybidae) ond author. No preserved parts. Eulophophyllum kirki Ingrisch Holotype designated from ‘Unfortunately E. kirki sp. n. could not be Valid. and Riede in Ingrisch et al. photograph. No pre- collected due to strict conservation rules 2016 (Insecta: Orthoptera: served parts. in the Danum Valley Conservation Area’ Tettigoniidae) (Ingrisch et al. 2016). Cheirogaleus shethi Frasier et al. Holotype captured, meas- Holotype and paratypes were all released. Valid. 2016 (Mammalia: Primates: ured, ear biopsies taken, Two older, preserved specimens were not Cheirogaleidae) blood sampled, micro- included in the type series. chip tagged, and speci- men released. Copyedited by: OUP
Insect Systematics and Diversity, 2017, Vol. 1, No. 1 11
Table 1. Continued
Taxon Types History Current status
Microcebus ganzhorni Hotaling Ear clip tissue sample A tissue sample of a released specimen, col- Valid. et al. 2016 (Mammalia: taken. No measurements, lected almost two decades ago, turned out Primates: Cheirogaleidae) photographs or morpho- to be genetically different from known logical data available. species. Holotype is preserved genomic DNA. Lepilemur otto Craul et al. Holotypes captured, pho- No full specimens were preserved because the Valid. 2017 (Mammalia: Primates, tographed, measured, novelty of the species was only discovered Lepilemuridae) ear biopsies and hair later in the lab. It was decided not to col- samples taken, specimens lect a specimen of this threatened species released. because of conservation and permitting issues (U. Radespiel, pers. comm. 2017). The species was first described by Craul et al. (2007) and considered valid in the literature (Zinner et al. 2007, Wilmet et al. 2014, Craul and Radespiel 2016). However, as the paper was published only electroni- cally at times when electronic publication was not permitted for nomenclatural purposes, the name was unavailable (Krell 2009) and was republished in a Code- compliant way by Craul et al. (2017). Lepilemur randrianasoloi, Holotype (L.r.)/syntypes No explicit reason for not preserving the full Valid. Lepilemur sahamalazen- (L.s.) captured, photo- holotype/syntypes is given in the paper, but sis Andriaholinirina et al. graphed, measured, ear the reasons are as above. The species were 2017 (Mammalia, Primates, biopsies taken, specimens first described byAndriaholinirina et al. Lepilemuridae) released. Tissue samples (2006) and considered valid in the litera- and DNA preserved ture (Zinner et al. 2007, Wilmet et al. 2014, Kappeler 2016, Seiler and Schwitzer 2016), However, as the paper was published only electronically at times when electronic publication was not permitted for nomen- clatural purposes, the names were unavail- able (Krell 2009) and were republished in a Code-compliant way by Andriaholinirina et al. (2017).
- studied, photographed and released, lost or never captured type No Preserved Type Material at All specimens (Fricke and Kacher 1982, Welch et al. 1986, Jonkers With the times of Linnaeus and Billberg long gone, new descrip- and Roersma 1990, Jones et al. 2005, Sinha et al. 2005, Mendes- tions without any preserved type material—without any physi- Pontes et al. 2006, Robb et al. 2013, Li et al. 2015, Marshall and cal evidence beyond photographs—appeared again in the 1980s. Evenhuis 2015, Lonsdale and Marshall 2016). The earliest example we know of is a deep water tilefish that - photographs or figures and previous descriptions used by authors was described by Fricke and Kacher (1982) on the basis of high- who have not personally studied or observed a physical speci- resolution footage from a submersible. Observed in depths of men, in contravention of Recommendation 73B (Billberg 1833, 80–116 m, specimens of this timid fish could not be caught. The Bock 1913, Wallach and Jones 1994, Hecq and Larsen 1998, authors were well aware that the set of morphological charac- Lowry and Springthorpe 2007, Bertagnolio and Racheli 2010, ters available for describing the new species was very limited as Nardelli 2015, Ingrisch et al. 2016); meristic characters (scale counts) could not be derived from the color slides. Indeed, when the species was used by Earle and Pyle The reasons, if stated, why no full specimens were preserved are (1997) for comparison with another new species of Hoplolatilus, - ethical or conservation considerations (Smith et al. 1991, Jones these shortcomings became obvious. While the body color, et al. 2005, Mendes-Pontes et al. 2006, Mishra and Sinha 2008 well documented on the photographs, indicates a distinct spe- [referring to Sinha et al. 2005], Gentile and Snell 2009, Barrera cies, morphometric and meristic characters could not be used et al. 2010, Robb et al. 2013, Li et al. 2015); comparatively. - legal obstacles (Peterson 2014 [referring to Athreya 2006], While the tilefish was actually observed by the authors who Ingrisch et al. 2016); extensively documented its behavior, some authors have pro- - capture technically impossible (Frike and Kacher 1982, Robb ceeded with descriptions on the basis of photographs of speci- et al. 2013); or mens they have not directly examined, thus disregarding Code - escape of the specimen (Marshall and Evenhuis 2015, Lonsdale Recommendation 73B that holotypes should be specimens studied and Marshall 2016). by the authors themselves. Copyedited by: OUP
12 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
Cryptophidion annamense, a snake from Vietnam, was described A new Strix owl was described from Oman by Robb et al. (2013) by Wallach and Jones (1994) on the basis of three almost 30-yr-old on the basis of photographs and sound recordings. Comparing their color slides. The authors published the detailed description in the photos with the poorly preserved holotype of Strix butleri and other journal Cryptozoology as they interpreted the lack of a preserved specimens identified as this species, they recognized two distinct spe- holotype as giving this species ‘cryptozoic status.’ Pauwels and cies and described one as the new species S. omanensis. The authors Meirte (1996) discussed the described characters and synonymized did not collect specimens because they considered the population the species with Xenopeltis unicolor Reinwardt, which was rebut- to be small, did not want to hamper the field study of the most eas- ted by Lazell (1996) and Wallach and Jones (1996). We are unsure ily accessible specimens, and assumed that permitting would have whether the community has reached a consensus about this species. been a problem. Two years later, Kirwan et al. (2015) recognized the A preserved specimen, or first-hand examination of the putative spe- same two species but considered the true S. butleri to be the species cies, might have helped to resolve the dispute. that Robb et al. called S. omanensis and considered S. butleri of In 2010, a new parrotlet from Colombia was described from Robb et al. to be an undescribed species. Kirwin et al. synonymized a photo of over 30 caged individuals found on the webpage of a S. omanensis with S. butleri and provided a new species name for wildlife recovery center. The center was unresponsive, and the web- S. butleri sensu. Robb et al. (2016) captured a specimen of that spe- site disappeared soon (Bertagnolio and Racheli 2010). The authors cies and collected feathers for DNA analysis, confirming Kirwan decided to describe and name the new bird as Forpus flavicollis et al.’s concept of S. butleri. Better type material might have helped because of its consistent and unusual coloration and fixed 31 of the with the resolution of this problem or might have avoided it in the 32 specimens in the photograph as syntypes. Shortly after publica- first place. tion of this new species, the ICZN Secretariat was notified about The most famous cases of descriptions from photos with the the case, and Notton (2011) clarified on behalf of the Secretariat deliberate decision to not kill and preserve full-body type specimens that the name was indeed available (i.e., legitimately published are descriptions of primates. Killing monkeys or lemurs for taxo- according to the Code). But Donegan et al. (2011) claimed that the nomic and nomenclatural purposes is widely considered unethi- specimens ‘seem very likely to have been individuals of [the com- cal, counterproductive to conservation efforts, and is often illegal, mon species] Spectacled Parrotlet Forpus conspicillatus with certain although blood or fur samples, for example, can and in most cases of their feathers dyed yellow or orange.’ Feather dying seems to be do serve as type material (e.g., Thalmann and Geissmann 2005; common in Colombia and particularly in this species. Donegan et al. Andriaholinirina et al. 2006; Louis et al. 2006, 2008; Zaramody synonymized the two species. With specimens at hand, the origi- et al. 2006; Craul et al. 2007; Olivieri et al. 2007; Radespiel et al. nal authors might not have been fooled or might have been able to 2008, 2012; Gentile and Snell 2009; Lei et al. 2015; Frasier et al. defend their interpretation if the color is natural. 2016; Hotaling et al. 2016). Jones et al. (2005) did not obtain The golden-crowned langur, Presbytis johnaspinalli, from such physical evidence prior to describing the highland mangabey Indonesia was described on the basis of five photographs of caged or kipunji, Lophocebus kipunji, from southern Tanzania on the specimens that had been posted to the Internet by conservation basis of two photographed specimens. A year later, a specimen and animal rescue organizations with very limited or no metadata was found dead in the trap of a resident farmer (Davenport et al. (Nardelli 2015). The photos show ‘one holotype and ten syntypes’ 2006). This specimen, now preserved in a museum collection, (which are in fact paratypes, not syntypes), all of a distinct colora- enabled further study of the species and led to a whole slew of tion. Later in the same year, as if the parrotlet history was repeating papers on phylogeny, morphology, and developmental biology and itself, Nijman (2015) pointed out that the new Presbytis species are its transfer into a different, new genus, Rungwecebus (Davenport ‘most likely partially bleached Ebony Langurs, Trachypithecus aura- et al. 2006). tus’, and probably the same specimens that were confiscated from In the same year, another monkey, Macaca munzala was described an Indonesian animal trader on the same day in 2009. Bleaching or from photographs (Sinha et al. 2005). Here, too, a specimen became dying mammals and birds to produce novelties for sale seems to be a available shortly after the original description but the taxonomic sta- common practice in Indonesian animal markets (Nijman 2015). The tus of the species remains unresolved (Biswas et al. 2011). original author defended himself promptly, questioning the practice The year after those two monkeys were described, a new spe- of artificially coloring in this case (Nardelli 2016). Subjective disa- cies of capuchin monkey, Cebus queirozi, was described by Mendes greements about species synonymy are routine even with the normal Pontes et al. (2006) from a forest remnant of about 200 ha in the availability of type specimens, but this particular issue could prob- Atlantic forest of Brazil, ‘at the very brink of extinction’. This one ably have been easily resolved if Nardelli’s description had been sup- was captured, measured, and comprehensively photographed before ported by preserved type material or at least by first-hand study of its release and without any part of the type specimen preserved. The the specimens in question. detailed description and documentation allowed de Oliveira and In earthworms, we have a case of a species first described in Langguth (2006) in the same year to determine the synonymy of C. an unpublished thesis but not formally published until over two queirozi with C. flavius (Schreber). decades later, after the type was lost. Dyne and Jamieson (2004) History repeated itself in 2015 when another monkey, Macaca write in the description of the new species Diplotrema glareaphila: leucogenys, was described from a large number of photographs (Li ‘As type specimens cannot be located, this species is erected on the et al. 2015), and a dead specimen was found at the time of the publi- illustration and account in Dyne (1984, unpublished [PhD thesis]) cation of the description. In the cases of these monkeys, the descrip- (ICZN 1999: Art. 73.1.4.).’ Such loss or potential loss can happen, tions all seemed a bit rushed since specimens became available very most likely after publication, but as we see, even before. The Code shortly after the photo-based descriptions. In case of the kipunji, the allows for such situations, as Art. 73.1.4. says: ‘Designation of an preserved specimen provided additional taxonomic insight, much as illustration of a single specimen as holotype is to be treated as des- the discovery of new material routinely permits new insights into the ignation of the specimen illustrated; the fact that the specimen no relationships of species known only from limited or older type mate- longer exists of cannot be traced does not of itself invalidate the rial. This, of course, is one of the reasons continued collection, even designation’ (ICZN 1999). of named species, is such a critical aspect of taxonomy. Copyedited by: OUP
Insect Systematics and Diversity, 2017, Vol. 1, No. 1 13
The above few examples from vertebrate taxonomy reflect a neotype], and that it may stimulate habitat protection measures for wide variations in taxonomic judgement—similar to the range these enigmatic species’. seen in the invertebrate literature—and incidentally illustrate the We see that taxonomic practice is and has been a continuum from obvious point that vouchers or types are highly desirable. The the vast majority of usual descriptions of new species with preserved normal course of taxonomic practice, including subsequent con- type material through to descriptions with living or very incomplete firmation or subsequent synonymy of species, can proceed in the type material and ultimately to exceptional and rare descriptions absence of type specimens just as it does with reference to type without any preserved type material. specimens of various quality. But quality preserved type mate- rial can often help in the resolution of ambiguities about species status. A Heated Debate, Triggered by a Fly or Two Marshall and Evenhuis (2015) raised the issue of proxy types in ento- How Will This Practice Affect Entomology? mology with a discussion of the pros and cons of species descriptions The recent increase in photo-based descriptions of vertebrates is in the absence of preserved type specimens. Their argument that unsurprising since ethical arguments against killing and preserv- ‘new species without dead bodies’ are occasionally justified triggered ing organisms are much more focussed on vertebrates than inver- a heated and unprecedented debate, resulting in the publication of tebrates. Nevertheless, a few cases of photo-based descriptions of an astonishing number of discussion and position papers, petitions, invertebrates exist, and one of them has triggered more debate than and polarized opinion pieces. all other photo-based descriptions combined. The debate started off on a collegial footing with point and In entomology, the first ‘photo-based’ description without a pre- counterpoint in the Bulletin of Zoological Nomenclature (Löbl et al. served specimen seems to be that of Bebearia banksi, a new spe- 2016, Marshall and Evenhuis 2016). Although many other issues cies of nymphalid butterfly from Ghana that was first detected on were discussed in these papers, we think the main points/counter- video tapes (Hecq and Larsen 1998). Bebearia banksi was later syn- points here and in the following debate were as follows: onymized with B. abesa Hewitson, 1869 due to an initial misinter- pretation of the intraspecific variation of this species (Larsen 2005). 1. A description without a preserved type is not science versus the The absence of a type had no bearing on this decision. description and naming of a new species represents a testable Then the unthinkable happened: A beautiful fly from South hypothesis whether or not the type is lost. Africa escaped after being photographed in detail, and the photo- 2. Any photograph can be easily modified or misinterpreted versus graphs showed that it was unequivocally a new member of a small specimens can be modified or misinterpreted, too. and distinct clade. Marshall and Evenhuis (2015) decided to describe 3. The absence of specimens prevents the discovery of additional this readily diagnosable fly as a new species, Marleyimyia xylocopae. characters versus more characters can be extracted from good What is more, they were outspoken about it, discussing the issue images than from bad specimens, and in any case, the discovery of and using some strong wording as an incentive for broader debate, new specimens (not re-examination of the type) normally leads to while advocating for the preservation of specimens whenever pos- the discovery of additional characters. sible. Broader debate they got. Starting with an opinion paper in 4. New species without preserved types should be named informally, Systematic Entomology authored by 14 (Santos et al. 2016), fol- not with a formal binomial versus if a species warrants naming, it lowed by a Zootaxa discussion paper signed by 50 authors (Amorim warrants naming under the rules of the Code. et al. 2016), the debate produced the Zootaxa paper (a petition) 5. Publications like Marshall and Evenhuis (2015) may stimulate with the largest number of signatories so far and for the time being: nonexperts to describe new species based on photographed speci- 493 (Ceríaco et al. 2016), and many papers to follow. This is remi- mens (i.e., produce nuisance descriptions) versus since the intrinsic niscent of the petition by Banks et al. (1993) who collected 98 sig- transparency of submitted papers with descriptions that are based natories from 19 countries speaking out against the descriptions of largely on photos will lead to an increased scrutiny by both edi- new bird species without preserved type specimens. But such peti- tors and reviewers, it should instead result in a drop in published tions represent politics and opportunism, not science, and have been nuisance descriptions. aptly described as ‘a facade of numbers’ by Warren and Bradford 6. Natural history collections will encounter further difficulties if (2013), who point out that ganging up against unpopular research decision-makers consider digitizing specimens to be an acceptable risks damaging scientific discourse and contributes little more than proxy for physical specimens versus Marshall and Evenhuis (2015) intimidation. made a strong case for collections and collecting, and the content In the midst of the current debate, Lonsdale and Marshall (2016) of their paper cannot be honestly used against collection support. described another distinct fly from a photograph. Their revision of the entire family Nothybidae included one distinctive species that These points of disagreement include the application of the Code they observed and photographed in the field but failed to collect. (point 4), opinions about taxonomic judgement (1, 3), and spec- Faced with the decision between ignoring it, naming it informally, or ulation about future actions by dishonest, inept, or incompetent giving it a proper name they chose to give it a proper name. Ingrisch individuals (2, 5, 6). These opinions were reiterated in a stream of et al. (2016) found themselves in a similar situation upon completion papers (Amorim et al. 2016, Ceríaco et al. 2016, Cianferoni and of their revision of the genus Eulophophyllum, a group of spectacu- Bartolozzi 2016, Krell et al. 2016, Pape et al. 2016, Faúndez 2017, lar pink katydids, for which species defining characters are clearly Garraffoni and Freitas 2017, Garrouste 2017, Gutiérrez and Pine visible on the photographs used in their revision. They were unable 2017, Löbl 2017, Nazari and Yanega 2017, Rogers et al. 2017, to obtain specimens of a distinctive species associated with threat- Thorpe 2017 and a whole issue of the journal Bionomina, see ened and strictly protected rainforest habitats and opted to name it Epstein 2017). The large number of papers did not contribute any- using a photo as a proxy with the expressed hope that it would ‘lead thing fundamentally new to the debate but clearly demonstrate that to further photographic and/or acoustic detections, that it will con- this controversial issue is of continuing interest to many practicing vince authorities to grant permits for collection of type material [i.e., taxonomists. Copyedited by: OUP
14 Insect Systematics and Diversity, 2017, Vol. 1, No. 1
The New Declaration of the ICZN Containing in circumstances when whole organism preservation is not feasible, Recommendations About Descriptions a portion (or portions) of the organism sufficient to allow the new Without Preserved Specimens species-group taxon to be reliably diagnosed should be preserved’ (ICZN 2017a). The issue of nonpreserved type material is not new, and comments In short: Photo-based descriptions are Code-compliant, but stating that such descriptions are available for the purposes of zoo- discouraged, or in the words of Marshall and Evenhuis (2015): logical nomenclature have been issued by the ICZN secretariat sev- ‘Specimens are indeed the ‘gold standard’ for species description’. eral times in the past (Wakeham-Dawson et al. 2002, Polaszek et al. However, in cases when specimens cannot be preserved, the Code 2005, Notton 2011). While these comments were in alignment with will not prevent taxonomy and Code-compliant naming to be the Code, they were not official declarations of the ICZN, hence executed. In such cases, authors of a new species or subspecies will could be disqualified as just being ‘personal opinions’ (Nemésio apply taxonomic judgement on a case-by-case basis to determine 2009). In March 2017, the ICZN issued a Declaration clarifying how to proceed. that unpreserved or lost type specimens do not affect the availability of names (ICZN 2017a). The ICZN considered the complex history of descriptions based on illustrations, with or without preserved Taxonomic Judgement type specimens, and practices in zoological disciplines dealing with The Code does not infringe on taxonomic judgment and does and organisms that are difficult or impossible to preserve. The previously will not regulate scientific reasoning and decisions. Not every taxon- published opinions of the former ICZN Executive Secretaries and omist exercises good judgment all the time, as most of us know from staff, of Donegan (2008), Marshall and Evenhuis (2016), and Pape et struggles with old (and some not so old) unrecognizable descrip- al. (2016) turned out to be in accordance with an official statement tions and out of context names. Fortunately, however, taxonomic of the ICZN. A Declaration cannot make major changes to the Code, standards are not timeless but change with advances in the repro- according to Code Art. 78.3.3. Thus the following (nonbinding) duction and dissemination of taxonomic information. Where once a Recommendations were issued to promote good taxonomic practice: few lines of text and an associated type were considered adequate, we now expect detailed descriptions with multiple images, careful Recommendation 73G. Specific reasons for designation of an unpre- dissections, and perhaps sequence data. But those expectations and served specimen as the name-bearing type. An author should the improving standards that lead to such expectations cannot and provide detailed reasoning why at least one preserved speci- should not be legislated by the Code. We cannot, for example, dictate men, whether a complete individual organism or a part of such that every description be accompanied by a dissection, a sequence, an individual, was not used as the name-bearing type for the or even a photograph because we cannot predict every circumstance new taxon and why the formal naming of the taxon is needed under which a taxonomist might deem a description appropriate. at a point in time when no preserved name-bearing type will be Compression fossils, amber specimens, deep-sea organisms, endan- available. gered vertebrates, and recognizable fragments all require different Recommendation 73H. Assertion of due diligence. When establish- sorts of taxonomic judgment under different circumstances. For ing a new species-group taxon without a preserved name-bearing example, only under very special circumstances would it be good type, steps taken by an author to capture and preserve a physical practice to name a single species known from a fragment or badly specimen of the new taxon and/or locate an existing preserved damaged specimen, but in the context of a complete revision, a tax- specimen in natural history collections should be recounted. onomist might confidently recognize a distinctive body part as a new Recommendation 73I. Consultation with specialists. Before the des- species that can be cast in the context of the revision. The Code can- ignation of an unpreserved specimen as a name-bearing type, an not dictate what quality or quantity of evidence is enough; that is a author should consult with specialists in the group in question. matter of taxonomic judgment. This judgment cannot get delegated Recommendation 73J. Comprehensive iconography and measure- to the ICZN (as suggested by Faúndez 2017), which governs nomen- ments. When establishing a new species-group taxon with- clatural rules but not scientific practice. out a preserved name-bearing type, the author should provide extensive documentation (e.g., multiple original high-resolution images, DNA sequences, etc.) of potentially diagnostic charac- Conclusions and Consensus ters as completely as possible. (ICZN 2017) Photographs, whether they are published on social media, amateur The Declaration contains the following explanatory note: ‘Whenever webpages, or just shared offline can be a rich source for new discov- feasible, new species-group taxa should be established on the basis eries. For example, a new species of green lacewing from Malaysia of at least one preserved type specimen. Additional information rep- was discovered on Flickr; the photographer was then encouraged resenting diagnostic characters (e.g., illustrations, DNA sequences, to search for another specimen that could be studied and preserved audio recording analyses, etc.) should accompany the description (Winterton et al. 2012). Film and photographic material taken in of a new species-group taxon whenever possible, but well-preserved a remote location ‘provided sufficient evidence to justify the col- biological specimens (either as complete individuals, or parts of lection of a type specimen’ of a new titi monkey species (Wallace individuals) are widely regarded as representing the most generally et al. 2006). A new mistletoe was discovered in photos compiled reliable means for establishing the biological and scientific basis for for an online checklist of Philippine vascular plants (Pelser and a species-group name. Establishing new species-group taxa without Barcelona 2013). The largest New World sundew and a pygmy devil preserved name-bearing type material is permissible under the Code (Tetrigidae) turned up on Facebook (Gonella et al. 2015, Skejo and but is discouraged unless justified by special circumstances, such as Caballero 2016). Skejo and Caballero then purchased specimens when capture or preservation of specimens is not feasible for techni- from a commercial dealer and linked up with collaborators in the cal reasons or for conservation concerns, or when specimens must Philippines who collected more specimens and obtained biological be destroyed to reliably diagnose a new species. While preserving a data. Gonella et al. organized a collecting trip to the origin of the whole organism as the type specimen is preferable and encouraged, photograph and obtained and preserved specimens. Copyedited by: OUP
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Sometimes efforts to collect and preserve physical specimens National Collection of Insects, Arachnids and Nematodes, Ottawa, Canada; might be fruitless or prohibited by law, or funding cannot be found Alain Dubois and Thierry Frétey, editors of Dumerilia, France; Maurice to revisit a remote region multiple times until a specimen is found Kottelat, Cornol, Switzerland; Sven Kullander, Swedish Museum of Natural or before the collecting locality has been destroyed. It is then up History, Stockholm, Sweden; Richard Pyle, Bernice Pauahi Bishop Museum, Honolulu, USA; Ute Radespiel, University of Veterinary Medicine Hannover, to the taxonomist’s judgment whether to proceed with a formal Germany; Geoff and Hilary Welch, La Bretonnière-La Claye, France. We description and naming without a preserved specimen. Some decide thank the editors of Insect Systematics and Diversity for inviting us to pen that the characters depicted in the photographs are sufficient for a this review. formal description and naming (Hecq and Larsen 1998, Marshall and Evenhuis 2015, Ingrisch et al. 2016, Lonsdale and Marshall 2016), others decide against it (Linke 2008a,b, Edwards et al. 2009, References Cited Madika et al. 2011, van der Heyden 2015). Aescht, E. 2008. Annotated catalogue of “type material” of ciliates (Ciliophora) A major point of criticism in the current debate was the fear that and some further protists at the Upper Austrian Museum in Linz, includ- encouraging photo-based descriptions by example could open the ing a guideline for “typification” of species. Denisia 23: 125–234. floodgates for descriptions without preserved type material (Amorim Amorim, D. S., C. M. D. Santos, F.-T. Krell, A. Dubois, S. S. Nihei, O. M. et al. 2016, Ceríaco et al. 2016, Cianferoni and Bartolozzi 2016). P. Oliveira, A. Pont, H. Song, V. K. Verdade, D. A. Fachin, et al. 2016. Not much time has passed, but so far, the feared flood of ‘fast and Timeless standards for species delimitation. Zootaxa 4137: 121–128. Andriaholinirina, N., J.-L. Fausser, C. Roos, D. Zinner, U. Thalmann, sloppy’ photo-based descriptions has not manifested itself, and we C. Rabarivola, I. Ravoarimanana, J. U. Ganzhorn, B. Meier, R. Hilgartner, know of only four recent examples of insects described using a photo et al. 2006. Molecular phylogeny and taxonomic revision of the sportive as a proxy for a lost or unpreserved type (Hecq and Larsen 1998, lemurs (Lepilemur, Primates). BMC Evol. Biol. 6: 17 (13 pp.). Marshall and Evenhuis 2015, Ingrisch et al. 2016, Lonsdale and Andriaholinirina, N., J.-L. Fausser, C. Roos, D. Zinner, U. Thalmann, C. Marshall 2016). The number and worldwide provenance of signa- Rabarivola, I. Ravoarimanana, J. U. Ganzhorn, B. Meier, R. Hilgartner, tories of the Ceríaco et al. petition opposing photo-based descrip- et al. 2017. Corrective paper concerning three new species of the genus tions indicates that many taxonomists expect that they will never Lepilemur Geoffroy, 1851 (Mammalia). Dumerilia 7: 62–71. need or want to describe a species using a photo as a proxy type. Andriantompohavana, R., J. R. Zaonarivelo, S. E. Engberg, R. Randriamampionona, Nevertheless, further carefully considered descriptions based on S. M. McGuire, G. D. Shore, R. Rakotonomenjanahary, R. A. Brenneman, ‘proxy types’ are likely to appear as some taxonomists complete and E. E. Louis. 2006. Mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occ. Pap. Mus. Texas revisions including species that are not represented by preserved Tech Univ. 259: 1–24. specimens, while at the same time, most practicing taxonomists are Andrianatompohavana, R., R. Lei, J. R. Zaonarivelo, S. E. Engberg, equipped with the tools to capture more and more data from living G. Nalanirina, S. M. McGuire, G. D. Shore, J. Andrianasolo, K. Herrington, specimens. We are, however, confident that descriptions without pre- R. A. Brenneman, et al. 2007. Molecular phylogeny and taxonomic revi- served types will be used judiciously and good taxonomic judgment sion of the wooly lemurs, genus Avahi (Primates: Lemuriformes). Spec. will prevail. Pub. Mus. Texas Tech Univ. 51: 1–59. Most participants in the recent debates agree that preserved spec- Athreya, R. 2006. A new species of Liocichla (Aves: Timaliidae) from Eaglenest imens should be the rule when describing new species or subspecies. Wildlife Sanctuary, Arunachal Pradesh, India. Indian Birds 2: 82–94. To reiterate the statement by Marshall and Evenhuis (2015): ‘Not Banks, R. C., S. M. Goodman, S. M. Lanyon, and T. S. Schulenberg. 1993. Type only do [specimens] allow for consideration of a full suite of char- specimens and basic principles of avian taxonomy. Auk 110: 413–414. Barrera, L. F., A. Bartels, and Fundación ProAves de Colombia. 2010. A new acters including internal morphology, microscopic, and genetic char- species of antpitta (family Grallariidae) from the Colibri del Sol Bird acters, they preserve data for future access with future technologies Reserve, Colombia. Conservación Colombiana 13: 8–24, front cover. and future questions. Specimen collections are our greatest treasure Bertagnolio, P., and L. Racheli. 2010. A new parrotlet from Colombia, Forpus trove of biodiversity information and continued collection develop- flavicollis. Avicult. Mag. 116: 128–131. ment must remain a priority.’ Purely photo-based descriptions of Billberg, G. J. 1833. Om ichthyologien och beskrifning öfver några nya new taxa of preservable animals must remain the rare exception, but fiskarter af samkäksslägtetSyngnathus . Linnéska Samfundets Handlingar they will remain admissible exceptions. We deplore growing restric- 1: 47–55, pl. tions on the collection of specimens and hope that such restrictions Biswas, J., D. K. Borah, A. Das, J. Das, P. C. Bhattacharjee, S. M. Mohnot, and do not increasingly force taxonomists to rely on new technology to R. H. Horwich. 2011. The enigmatic Arunchal macaque: its biogeography, produce descriptions without preserved types. biology and taxonomy in northeastern India. Am. J. Primatol. 73: 1–16. Bock, S. 1913. Studien über Polycladen. Zool. Bid. Uppsala 2: 31–343, pls 3–10. Note Böhme, W. 2014. Herpetology in Bonn. Mertensiella 21: I–VI, 1–256. Böhme, W., and T. Ziegler. 1997. Varanus melinus sp. n., ein neuer Waran aus Frank-T. Krell is a Commissioner and Councillor of the International der V. indicus-Gruppe von den Molukken, Indonesien. Herpetofauna 19: Commission on Zoological Nomenclature and has chaired the committee that 26–34. drafted Declaration 45. The draft of the Declaration was then extensively dis- Brown, B. 1987. Two new anabantoid species. Aquarist and Pondkeeper June cussed and modified by the whole Commission before it was issued. 1987: 34. Carantón-Ayala, D., and K. Certuche-Cubillos. 2010. A new species of antpitta (Grallariidae: Grallaria) from the northern sector of the Western Andes of Acknowledgments Colombia. Ornitología Colombiana 9: 56–70. Several people helped with gathering examples of or background information Ceríaco, L. M. P., E. E. Gutiérrez, A. Dubois, and 490 additional signatories. to descriptions based on unpreserved types, either when the senior author led 2016. Photography-based taxonomy is inadequate, unnecessary, and the drafting of the ICZN Declaration 45, or when we worked on this paper: potentially harmful for biological sciences. Zootaxa 4196: 435–445. Erna Aescht, Biology Centre of the Upper Austrian Museum, Linz, Austria; Cianferoni, F., and L. Bartolozzi. 2016. Warning: potential problems for tax- Alberto Ballerio, Brescia, Italy; George Beccaloni, Alfred Russel Wallace onomy on the horizon? Zootaxa 4139: 128–130. Correspondence Project, London, UK; Wolfgang Böhme, Zoological Research Collar, N. J. 1999. New species, high standards and the case of Laniarius Museum Alexander Koenig, Bonn, Germany; Patrice Bouchard, Canadian liberatus. Ibis 141: 358–367. Copyedited by: OUP
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