Published by Associazione Teriologica Italiana Online ﬁrst – 2013
Hystrix, the Italian Journal of Mammalogy
Available online at:
Mammal taxonomy without taxonomists: a reply to Zachos and Lovari
, Fenton P.D. Cotterillb, Colin P. Grovesc
aViale Liegi 48A, 00198 Roma, Italy
bAEON – Africa Earth Observatory Network, Geoecodynamics Research Hub, c/o Department of Botany and Zoology, University of Stellenbosch, Stellenbosch 7602, South Africa
cSchool of Archaeology & Anthropology, Australian National University, Canberra, Australia
polytypic species concept
Received: 20 April 2013
Accepted: 24 April 2013
Ontological and epistemological properties of the Phylogenetic Species Concept (PSC) as applied
in recent mammalian taxonomic works are redeﬁned and defended against criticisms raised by
Zachos and Lovari (2013), which we ﬁnd inapplicable to taxonomy because they relate more to the
ﬁeld of population biology. We summarize the negative impacts of the polytypic species concept
for conservation and evolutionary biology, with emphasis on Rhinocerotidae. The priority need to
embrace and strengthen museum-based taxonomic research is emphasized.
The reply of Zachos and Lovari (2013) to our previous opinion pa-
per (Gippoliti and Groves, 2012) provides us with the opportunity to
expand our argument.
In 2011 three putative “subspecies” of the family Rhinocerotidae
were declared oﬃcially Extinct by IUCN: the western black rhinoceros
Diceros bicornis longipes Zukowsky, 1949; the Nile white rhinoceros
Ceratotherium simus cottoni (Lydekker, 1908) (with a handful of in-
dividuals surviving in captivity); and the Indochinese Javan Rhino-
ceros Rhinoceros sondaicus annamiticus Heude, 1892. We contend
that Zachos and Lovari’s reply (2013), and other similar papers (Heller
et al., 2013; Zachos et al., 2013a,b), are missing the core point. The
taxonomic approach they are defending has some responsibility for the
demise of so many unique forms of rhinoceros in Africa and Asia. The
raising of cottoni to speciﬁc level by Groves et al. (2010) is based more
on new data (and we should add real interest in a too long forgotten
question) than a shift in the species deﬁnition adopted. The Nile white
rhinoceros deserves species status on any or all species criteria, and
we fear that a demonstration of this would be apparent if interbreeding
with the southern species will be attempted as a last hope to “save” it.
Although even more poorly known due to their historic rarity, and the
consequent scarcity of study material, the same predicament may well
apply to Diceros bicornis longipes and Rhinoceros sondaicus annam-
iticus. Here knowledge of the palaeoclimatological and geomorpho-
logical history of both continents (Cotterill, 2003a; Whitmore, 1987;
Kingston, 2007; Senut et al., 2009), together with comparative phylo-
geographic studies of extant biogeographic patterns, strongly suggest
that these now extinct rhinoceros taxa actually constituted distinct spe-
cies. If we look at recent proposals of giraﬀe taxonomy, for instance
(Brown et al., 2007; Groves and Grubb, 2011), all recognize speciﬁc
status for the West-central African taxa that occurred sympatrically
with Diceros longipes and remained isolated from eastern populations.
This possibly related to an important barrier: Lake Megachad (Has-
sanin et al., 2007). We are not proposing a formal taxonomic revision,
which of course would require detailed research; but we would like
to draw attention to how – as exempliﬁed by Roberts’ Lechwe Kobus
robertsi and Upemba Lechwe Kobus anselli (Cotterill, 2003b, 2005)
Email address: firstname.lastname@example.org (Spartaco Gippoliti)
– a taxon becomes nearly invisible to conservation when it is “only a
That said, we note that the cases cited by Zachos and Lovari (2013)
actually contradict, not support, their fear (Zachos et al., 2013a) of the
PSC as applied by Groves and Grubb (2011). Their Fig. 1 clearly shows
that species in the Cervus elaphus complex form monophyletic clades,
exactly as maintained by Groves and Grubb (2011) on the basis of com-
mon morphological characters. The fact that monophyletic lineages ex-
ist within each of these three clades (some of them picked out by roun-
ded squares in Zachos and Lovari’s (2013) Fig. 1) is irrelevant: Zachos
and Lovari appear to have forgotten that the species, however deﬁned,
is a population concept (“a population or aggregation of populations” –
Groves and Grubb 2011:1). And indeed this fundamental ontological
nature of the species category was emphasized on the opening page
of Groves and Grubb 2011:1: ”a lineage . . . evolving separately from
others and with its own evolutionary role and tendencies” (Simpson,
1961), which is operationalized by the PSC (Cotterill, 2003b, 2005;
Groves and Grubb, 2011).
We emphasize that the concept of evolutionary species is a cent-
ral ontological foundation of phylogenetic systematics; the species-
as-lineage concept of the ESC (Evolutionary Species Concept) struc-
tures discovery operations – using the PSC and relevant evidence – to
characterize those lineages that qualify as individuated species. The
realm of organismal more-making , the tokogenic processes that create
populations, occupies the hierarchical level below that where species
evolve, persist and go extinct (Hennig, 1966; Frost and Kluge, 1994).
Zachos and Lovari are broadly correct that events testifying to the cir-
cumstances of lineage scission can be challenging to elucidate – but
this ontology accommodates such apparent conﬂicts in evidence (de
Queiroz, 2007; Mayden, 2013). At its most fundamental, this is the
nature of biodiversity resplendent in the one tree shaped by the gene-
alogical history of life on earth, and it evolved independently of our
ability to discover its topology. Alongside the realities of hypothesis-
driven biological research, this singularity obviates the credibility of
dividing or lumping organisms into artiﬁcial groups (Darwin, 1859;
O’Hara, 1988; Brooks and McLennan, 2002; Naomi, 2011; Wiley and
Lieberman, 2011; Mayden, 2013).
Again, this failure to understand the ontological context of how the
PSC is applied in the lineage framework of the ESC (cf. Cotterill
2003b, 2005) is revealed in their Fig. 2 and text (Zachos and Lovari,
Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 29th April 2013
2013 Associazione Teriologica Italiana
Hystrix, It. J. Mamm. (2013) — online ﬁrst
2013), which focus on recent population fragmentation – with the In-
dian tiger Panthera tigris tigris as an example – and its possible genetic
consequences. Previously Zachos et al. (2013a) had heavily criticized
a three-species arrangement of tigers (Groves and Mazák, 2006) res-
ulting from the complex history of the Sunda Shelf and its sequence
of separation from and reconnection with mainland Asia in the Qua-
ternary (Michaux, 2010). Indian tigers may likewise present genetic
and morphological substructuring over their formerly vast range, and
this is as likely to be maintained by contemporary ecological processes
as by drift, as has been shown for boreal grey wolves (Musiani et al.,
2007). If today’s remnant isolates are discovered to be strongly diﬀer-
entiated genetically, it is likely to be initially a legacy of this previous
substructuring, even if drift later modiﬁes populations, and it is import-
ant that such processes should be considered in conservation strategy.
Unfortunately, too many translocations of wildlife have had detrimental
eﬀects on the conservation of biodiversity by introducing alien genetic
material (Champagnon et al., 2012) because they are misled as a con-
sequence of prevalent taxonomic views based on the Biological Species
Concept (BSC) (Gippoliti, 2004).
We further argue that setting draconian restrictions on the evid-
ence judged suﬃcient to characterize species underestimates cryptic
diversity, especially where such actions seek to reduce “taxonomic in-
ﬂation” (Bernardo, 2011). The argument that “If an independent evol-
utionary history, i.e. largely separate gene pools, is what ultimately
makes a species, then conclusive nuclear genetic or mitochondrial and
nuclear genetic data is what should be required from geneticists be-
fore splitting a species” (Zachos et al. 2013a: 5) violates the Precau-
tionary Principle in cases of some real species. Even a surfeit of gene
trees can still fail to discover some recently diverged species (Arnold
et al., 2013). These include lineages that (1) were founded by hybrid-
ization, (2) have experienced introgression, and/or (3) retain ancestral
polymorphisms (Norris and Hull, 2011).
In summary, criticism of excessive use of the diagnosability criterion
is unwarranted, not least for Groves and Grubb (2011), who maintained
subspeciﬁc taxa against PSC criteria.
We share the concern against non-peer-reviewed taxonomic de-
cisions (cf. Kaiser et al. 2013) but we maintain the importance of mu-
seum based taxonomy to oﬀer solutions even with limited specimens
at hand – this Precautionary Principle sets the rule for little-known and
threatened taxa. Here, we emphasize that the overwhelming advant-
age that the PSC has over any other species concept is its testability;
the accumulation of further evidence can falsify a taxonomic statement
under the PSC. This is a requirement for a credible scientiﬁc proposi-
tion (Bernardo, 2011). As an historical example from before the advent
of the BSC, we highlight the pioneering revisions of Lorenzo Camer-
ano (1856-1917), director of the Zoological Museum at Turin Univer-
sity. Camerano stands out for introducing mathematical methods in
taxonomy and ecology (cf. Cohen 1994) and for studying species vari-
ability with large museum samples, in particular skulls, in his studies
of Rupicapra and Capra ibex taxonomy. In one of his last papers he
lamented the abuse of the subspecies category in several bovid species
(Camerano 1916: 4). In a little-known paper, he (Camerano, 1917)
challenged the validity of the taxonomic arrangement of the Iberian
ibexes proposed by Cabrera (1911: one species and four subspecies);
he proposed, on the basis of published data, and the study of two further
specimens in the Turin Museum, the existence of two distinct species,
Capra pyrenaica and Capra hispanica, with three subspecies possibly
of ancient hybrid origin (Camerano, 1917). This little-appreciated pa-
per (but see García-González 2011) oﬀers an excellent example of a
phylogenetic approach to classical taxonomy, and is all the more per-
tinent today to inform conservation policies of threatened mammal pop-
It is important to reconcile with the circumstances that the BSC
(Mayr, 1963) and the Genetic Species Concept (Baker and Bradley,
2006) are constrained by operational strictures as to where a species
“appears” in the process of lineage individuation. It is indeed unclear
how the BSC can actually discover lineages in the framework of phylo-
genetic systematics. Only the ESC is free of these operational strictures
(Frost and Kluge, 1994; Mayden, 2013). The poverty of operational-
ism and its primal failure of systematics was refuted over forty years
ago (Hull, 1968; Johnson, 1970; Frost and Kluge, 1994):
...the operational point of view depends for what success it
does have on the very element of science which it is designed
to eliminate. Operationism was intended as a cathartic to
purge physics of all non-empirical wastes, but it proved to
be so strong that the viscera were eliminated as well. (Hull
An extreme version of operationalism has appeared in the Diﬀerential
Fitness Species Concept (DFSC) of Hausdorf (2011) – unfortunately
lauded by Frankham et al. (2002) in a recent publication – which has
tried to avoid the species-are-lineages ontology. This stricken attempt
to exhume a sterile research program removes the concept of the pop-
ulation from the deﬁnition of the species category; the DFSC strips
science of the reality of population biology, and ignores the hierarch-
ical organization of biodiversity, represented in the singular species tree
that systematics is challenged to discover. We are unconvinced by this
strange attempt to overturn a fundamental foundation of evolutionary
biology. Ultimately, all these attempts to dismiss the PSC (Frankham et
al., 2002; Heller et al., 2013; Zachos et al., 2013a,b; Zachos and Lovari,
2013) are crippled by operationalism. It is unfortunate that this ret-
rogressive perspective is held up as the way forward for conservation
policy, considering that the bioGenesis research strategy founded on
phylogenetic systematics (Donoghue et al., 2009; Hendry et al, 2010)
was developed expressly to guide policy formulated by the Conference
of the Parties (COP) to the Biodiversity Convention.
In the light of the consolidation of phylogenetic systematics and its
demonstrable progress toward discovering the singular Tree of Life
(Bernardo, 2011; Wiley and Lieberman, 2011; Mayden, 2013), all other
pretenses at dividing or lumping organisms into artiﬁcial taxonomic
groups can no longer be defended, at least on scientiﬁc grounds. Con-
servation costs of taxonomic mistakes can be extreme. We cited these
historical examples to stress the need to integrate old and new method-
ologies for the study of mammal diversity – before it is also too late, and
more taxa meet the same plight exempliﬁed by Ceratotherium cottoni.
Especially in Western Europe, demands for knowledge, and improve-
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