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Impacts of taxonomic inertia for the conservation of African ungulate diversity: An overview

Authors:
  • Società Italiana per la Storia della Fauna "Giuseppe Altobello"

Abstract

We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of the polytypic species concept and the discipline's general neglect since the middle of the 20th century. We single out negative consequences of 'orthodox' taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements caused by involuntary lineage mixing. We advocate that specimen-based taxonomy should regain its keystone role in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity, we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups of 'utilizers' such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that purported 'taxonomic inflation' has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural resource.
Biol. Rev. (2017), pp. 000000. 1
doi: 10.1111/brv.12335
Impacts of taxonomic inertia for the
conservation of African ungulate diversity:
an overview
Spartaco Gippoliti1, Fenton P. D. Cotterill2, Dietmar Zinner3,and Colin P. Groves4
1Societ`a Italiana di Storia della Fauna ‘G. Altobello’ Viale Liegi 48, 00198 Roma, Italy
2Geoecodynamics Research Hub, Department of Earth Sciences, University of Stellenbosch, Stellenbosch 7602, South Africa
3Cognitive Ethology Laboratory, German Primate Center, 37077 G¨ottingen, Germany
4School of Archaeology & Anthropology, Australian National University, Canberra, Australia
ABSTRACT
We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of
the polytypic species concept and the discipline’s general neglect since the middle of the 20th century. We single out
negative consequences of ‘orthodox’ taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound
translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic
infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements
caused by involuntary lineage mixing. We advocate that specimen-based taxonomy should regain its keystone role
in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While
integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity,
we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups
of ‘utilizers’ such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that
purported ‘taxonomic inflation’ has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has
such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable
management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural
resource.
Key words: conservation, morphological diversity, hybridization, phylogenetic species concept, extinct taxa, sustainable
utilization.
CONTENTS
I. Introduction .............................................................................................. 2
II. Historical perspective on ungulate taxonomy in Africa ................................................... 2
(1) The genesis of ungulate taxonomy ................................................................... 2
(2) Molecular contemporary approaches ................................................................. 4
(3) Why ‘taxonomic inflation’ is a misnomer ............................................................. 4
III. Taxonomic inflation and conservation ................................................................... 6
IV. Translocation ‘rescue’ and conservation genetics ......................................................... 7
V. The role of hybridization in species concepts and conservation .......................................... 9
VI. How can a ‘new alpha taxonomy’ support conservation? ................................................ 10
(1) Forgotten taxa, forgotten hotspots .................................................................... 10
(2) Taxonomic impacts on the wildlife industry and sustainable conservation ........................... 10
(3) How precise and accurate taxonomy informs a hierarchical conservation strategy ................... 11
VII. Conclusions .............................................................................................. 12
VIII. Acknowledgements ....................................................................................... 12
IX. References ................................................................................................ 12
* Address for correspondence (Tel: +49 551 3851129; Fax: +49 551 3851372; E-mail: DZinner@dpz.eu).
Biological Reviews (2017) 000– 000 ©2017 Cambridge Philosophical Society
2S. Gippoliti and others
I. INTRODUCTION
Conservation biology requires taxonomy for sound scientific
guidance. Taxonomic errors have negative impacts on
accurate and precise knowledge of species diversity; these
errors can mislead conservation evaluations and misinform
characterizations of biogeographical history (Adams, 1998;
Bernardo, 2011; Cotterill et al., 2014). The taxonomic
impediment (Hoagland, 1996) compounds these challenges,
so that better surveyed taxa – pertinently vertebrates – are
relied on as surrogate indicators to assess biodiversity,
notably in gap analyses evaluating protected area coverage.
Moreover, conservation assessments increasingly employ
estimates of phylogenetic distinctiveness (PD) to characterize
historical attributes of taxa to identify biodiversity hotspots.
PD estimates expand the traditional focus beyond
quantifying extant population diversity to incorporate
evolutionary histories of biota across landscapes and
continents (King, 2009).
Remarkably, and notwithstanding earlier revisions of a few
species complexes (Cotterill, 2003a,b, 2005), until recently
the classification of ungulates (hoofed mammals belonging to
the orders Artiodactyla and Perissodactyla) remained almost
unchanged from the middle of the 20th century. We here use
the term ‘taxonomic inertia’ to describe this persistence of
incomplete knowledge of biodiversity. Fortunately, the tax-
onomy of ungulates underwent wholesale revision recently
(Groves & Grubb, 2011; Groves & Leslie, 2011) leading
to a considerable increase in the number of recognized
species. Interestingly, this revised classification systematically
employs the phylogenetic species concept (PSC) to opera-
tionalize the evolutionary species concept (ESC) [the former
name for the general lineage concept (GLC) of de Queiroz
(1999)]. The application of the ESC has been criticized as
‘taxonomic inflation’ (a term first used by Isaac, Mallet &
Mace, 2004) in recognizing too many false species (Type
I errors) (Cotterill et al., 2014). These criticisms invoke two
main issues: first, recognizing ‘too many species’ has negative
consequences for conservation biology in that it impedes
human-assisted gene flow (e.g. through restocking programs)
between threatened ‘populations’, when the latter are consid-
ered to be distinct species (Frankham et al., 2012; Heller et al.,
2013; Zachos et al., 2013a,b). Second, given insufficient fund-
ing for biodiversity conservation, an increase in the number
of recognized species reduces the resources available per
threatened species and thus aggravates the ‘agony of choice’
for conservation planners and managers (Isaac et al., 2004;
Collen et al., 2011). Respondents to both criticisms argue that
understanding mammalian diversity must be guided by the
best available scientific framework within the available evi-
dence, and condemn artificial lumping of species because it
undermines biodiversity assessments, especially where plan-
ners rely on recognized species of ungulates as surrogate
indicators and/or flagships in conservation planning (Gip-
politi, Cotterill & Groves, 2013; Cotterill et al., 2014).
Taxonomic inertia raises critical questions. What are its
impacts? In particular, how has taxonomic inertia influenced
not just past decisions but prevailing policy? And for the
ungulates, why has this debate been so delayed, compared
to the other main branches of vertebrate taxonomy, and
what are the consequences of this for understanding African
ungulate diversity, a unique heritage of this continent?
Here we review the history of ungulate taxonomy
to highlight how taxonomic inertia has propagated the
remarkable prevalence and persistence of taxonomic errors.
Presenting this long-overdue historical context explicates the
polarized points of view that shaped the major taxonomic
syntheses of African ungulates over the last 120 years. These
trends and tensions in taxonomic knowledge further (i)
distinguish between taxonomic revisions versus reviews, and
(ii) underscore the fundamental roles of available hypodigms
on which derived taxonomies ultimately stand or fall. Above
all, we show that impacts of taxonomic errors on conservation
are hard-hitting, and we highlight problems exacerbated by
the mixing of different populations of African ungulates,
in the wild and the semi-wild as well as in captivity.
These undermine the credibility of repeated translocations
of ungulate ‘species’.
II. HISTORICAL PERSPECTIVE ON UNGULATE
TAXONOMY IN AFRICA
(1) The genesis of ungulate taxonomy
Until the end of the 20th century, an established consensus
believed that the living African ungulates comprised 95
recognized species, three of which became extinct recently
(summarized in the compilation of Corbet & Hill, 1986),
and it followed that the goal to maintain the diversity of
ungulate species in Africa was not a ‘mission impossible’. This
‘orthodox’ taxonomy, originating in reviews and checklists
(not true taxonomic revisions) of the 1930s, 1940s and 1950s,
had come to be perceived as definitive by the scientific
community. This tacit belief coincided with a general decline
of interest in researching mammal collections, especially in
Western European museums. Here, we define ‘orthodox’
taxonomy as the classification derived from the taxonomic
reviews of Allen (1939); Ellerman & Morrison-Scott
(1951) and Ellerman, Morrison-Scott & Hayman (1953),
which classified previously described mammals using a
polytypic species concept [biological species concept (BSC)
or morphological species concept (MSC)]. Over the
following decades, and despite the addition of little, if
any, empirical evidence, the taxonomic arrangements in all
three monographs have been unquestioningly accepted and
utilized, and often perceived as ‘definitive’ by users, leading
to decades of taxonomic inertia (Gippoliti & Groves, 2012).
The low contemporary appeal of mammalian taxonomy
meant that few biologists scrutinized ungulate diversity,
unlike the attention paid to the more speciose small mammals
such as Rodentia and Chiroptera, even when new potential
material and data were available. Thus Cuneo (1965), for
example, while describing the breeding at Naples Zoo of
Biological Reviews (2017) 000– 000 ©2017 Cambridge Philosophical Society
Taxonomic inertia and ungulate conservation 3
Abyssinian klipspringers Oreotragus saltatrixoides,reportedthat
of the four founder individuals, the two received from the
AsmaraKeren area had a chestnut-grey pelage, while the
two from Senafe had a grey-brown pelage. This remarkable
observation – on antelopes originating from within the same
country, within a distance of less than 150 km corroborates
evidence of geomorphological controls on diversification of
Ethiopian large mammals (cf . Gippoliti, 2010). It is unlikely
that any of these Naples klipspringer founders was deposited
and appropriately labelled in a museum after death – yet
another example of taxonomic neglect (Cotterill & Foissner,
2010).
In the 1980s, the first quantitative genetic studies identified
an important potential problem for conservation biology.
Evaluations of captive populations (such as those of dorcas
gazelle Gazella dorcas) revealed deficient genetic variation and
heterozygosity, highlighting potentially insidious inbreeding
depression (Ralls, Brugger & Glick, 1980). This study served
to reinforce the prevailing concept of ‘biological species’,
and the conclusion was drawn that the interbreeding
of geographically separated populations purportedly of
the same species would increase genetic variation to
minimize the negative effects of inbreeding (Frankham
et al., 2012). While Speke’s gazelles Gazella spekei were used
as a model for the elimination of inbreeding depression
from a small captive stock (Templeton & Read, 1998),
another African mammal, the cheetah Acinonyx jubatus,
was found to exhibit apparently abnormally low genetic
diversity (O’Brien et al., 1985), and in this case interbreeding
between southern and eastern African individuals was
suggested as a possible countermeasure (irrespective of
potential outbreeding depression). Considered in hindsight,
preliminary population genetics data together with a
simplistic understanding of the small-population paradigm
(cf . Caughley, 1994) not only exerted a strong influence
on thinking among conservation professionals, but also
moulded policies toward the perceived sustainability of
animal populations – not only in ex situ situations but also in
protected areas. The case of dwindling species has received
high-profile attention.
Significantly, the historical trend towards lumping
ungulate species has been compounded by abuse of the
subspecies category. Perhaps this was favoured by the
impressive flood of mostly spurious ‘species’ by some
late-19th century taxonomists such as Paul Matschie in
Berlin, which were often based on single individuals as well as
on metaphysical theories about the geographical distribution
of species along river basins rather than objective analyses
of variation of morphological characters. It was perhaps
as a counterbalance that other mammalian taxonomists
turned with enthusiasm to the trinomial, following the
lead of Lord Rothschild and his colleagues (Rothschild,
Hartert & Jordan, 1903; and see Mallet, 2004). Thus
Lydekker (1913, p. vi) already adopted ‘to a great extent
the principle of classing nearly related kinds of animals as
races of a single species rather than as distinct species ...’,
and, accordingly, classified the African buffaloes as a single
species, Bos [now Syncerus] caffer, with 21 subspecies. Ernst
Schwarz followed the same path of simplification at the
species level – as in his paper on duikers and in his otherwise
seminal paper on Alcelaphus (Schwarz, 1914; Ruxton &
Schwarz, 1929). Rothschild himself contributed to the
spread of the trinomial in mammalian taxonomy, describing
numerous new ‘races’ (meaning subspecies) of ungulates (e.g.
Rothschild, 1921). It is possible that accepting subspecies
in a polytypic species served to lower the responsibility
for the taxonomist’s decision, but it is interesting that
already in 1916 this trend to recognize too many ungulate
subspecies despite only one (or few) specimens, and without
valid morphological characters, was criticized by some (e.g.
Camerano, 1916). As a taxonomic category, the subspecies
concept became a panacea to deal with problematic
situations: especially to characterize differing patterns of
morphological variation in (apparently) closely related
populations. In reality, conversely to the polytypic species
ideal, such variation could represent a population within a
metapopulation or a divergent lineage lacking unambiguous
evidence (morphological at least) of distinct evolutionary
independence.
In important respects, Schwarz was pioneering an
evolutionary approach in mammal taxonomy, especially in
his Alcelaphus paper (Ruxton & Schwarz, 1929), which was
part of a series entitled Stages in the Evolution of Species.After
publication of the influential books of Dobzhansky (1937);
Huxley (1940) and Mayr (1942) advocating the BSC, and
following the lead of Allen (1939), mammalogists at the then
British Museum (Natural History) seemed to take it as their
duty to revise the mammal checklists of the Old World
mammals in light of the New Systematics and the BSC
(Ellerman & Morrison-Scott, 1951; Ellerman et al., 1953).
Judging from at least two critical book reviews (Handley,
1954; Ansell, 1958a), the immediate response to Ellerman
and colleagues was that they had gone too far in lumping
‘species’ of Old World mammals. One reviewer of their
Mammals of Southern Africa (Ellerman et al., 1953) observed:
‘‘Their ‘species’ is frequently equal to the ‘species group’
of American taxonomists. It often appears that to them the
criterion of conspecifity is gross resemblance, demonstration
of intergradations is unnecessary, and broad overlap of
ranges of ‘subspecies’ is an unimportant detail’’ (Handley,
1954, p. 460).
For decades, until the molecular biology revolution, a
general neglect undermined characterization of challenging
and/or cryptic diversity at the species level in vertebrates.
It was compounded over the next half century, because
taxonomy became ‘out of fashion’ and museum-based
research programs became limited in number and scope,
especially in Western Europe. The widespread negative
trends across comparative biology over this period hit
taxonomy hardest in what Brooks & McLennan (1999,
2002) term the ‘Eclipse of History’ (cf . Cotterill, 2016).
As a consequence of this dearth of studies of the major
museum collections of large mammals, non-specialists tended
to assume that the taxonomy of these groups was resolved
Biological Reviews (2017) 000– 000 ©2017 Cambridge Philosophical Society
4S. Gippoliti and others
and definitive. Species boundaries were treated as firmly
set. Moreover, it was believed that little if any diversity
awaited discovery, especially of large mammals. Illustrative
of this viewpoint was the reduction to a care and maintenance
policy of the avian and mammalian collections of the Natural
History Museum in London after 1989, recounted by Fortey
(2008). Viewed today in the context of the prevailing scientific
paradigm, there were few tentative advances through the
latter half of the 20th century, and only a few descriptions
of new taxa, such as the Nigerian pygmy hippopotamus
Choeropsis liberiensis heslopi by Corbet (1969), occasionally
broke through this ominous stagnation.
Since the beginning of the 21st century, a number of
more easily recognizable, geographically isolated lineages
have been rehabilitated as distinct species. Thus, Grubb
(1993, 2005) recognized 100 and 101 species of African
ungulates, respectively, in the two editions of Mammal Species
of the World. In the meantime Cotterill (2000, 2003a,b, 2005)
questioned the validity of the BSC to describe ungulate
diversity in Africa; he advocated the ESC as the only
valid solution to discover and describe the true diversity
of African antelopes, and also reiterated major problems
and challenges in mammalogy identified decades earlier by
Ansell (1958b). Even if all data from ungulate collections
of the major museums were collated – assembled from
across the globe their hypodigms remain inadequate.
This general lack of specimens continues to weaken
quantitative comparisons of inter-demic variation to
inform modern, geographically representative taxonomic
revisions.
(2) Molecular contemporary approaches
One might have expected molecular evidence to help
solve these taxonomic inadequacies. Instead, it appears
the challenges of characterizing ambiguous morphological
variation have endured for decades, despite the grand
promises of molecular genetics since the 1950s: first
karyology, then electrophoresis and more recently estimates
of genetic variation from directly sequencing the genome.
The latter began with random amplification of polymorphic
DNA (RAPD) and related restriction-enzyme comparative
mapping, then mitochondrial DNA sequencing, inaugurated
by Avise and collaborators in the late 1980s (Avise, 2000),
and most recently comparative genomics. The most recent
suite of methods enabled by high-throughput sequencing
methods exemplified in restriction site associated DNA
sequencing (RADSeq) (Ekblom & Galindo, 2011) – enables
hitherto unprecedented characterization of genomic
variation. RADSeq has begun to be used in generic revisions,
where it vindicates earlier estimates of the widespread
incidence of cryptic species. This is underscored by the
exemplary taxon sampling in a recent study of African
guenons, including many subspecies, synonymized decades
earlier; comprehensive genomic evidence evaluated using
RADSeq now demonstrates that these subspecies are
evolutionarily independent lineages (Guschanski et al., 2013).
Prior to the recent invention of high-throughput
sequencing, exemplified in RADSeq, pioneering studies of
genetic diversity of the Bovidae (e.g. Arctander, Johansen &
Coutellac-Vreto, 1999; Matthee & Robinson, 1999; Alpers
et al., 2004; Lorenzen, Heller & Siegismund, 2012) relied on
mitochondrial DNA (mtDNA) variation and microsatellites
as genetic markers. With the exception of the continental
overview of the Tragelaphus scriptus and T. sylvaticus complexes
(Moodley & Bruford, 2007), these preserved the conservative
taxonomy of Allen (1939) and Ellerman et al. (1953). Actually,
uncritically or otherwise, these authors assumed the reality
of these ‘species’, and did not test species boundaries.
The common deficiency is the failure of these studies to
explicitly genotype topotypical populations of all described
subspecies; it is then impossible to anchor phylogeographical
findings on the known taxonomic framework. Nearly all
phylogeographers continue to evaluate ungulate diversity
under a polytypic species concept. This widespread failure
to evaluate species boundaries critically in an explicit
phylogenetic framework is strange, and raises questions
considering expansion of tree-thinking philosophy (sensu
O’Hara, 1988) into conservation theory (e.g. Erwin, 1991;
Vane-Wright, Humphries & Williams, 1991), and increasing
investments prioritizing characterization of the evolutionary
dimensions of biodiversity in biodiversity assessments and
policy (Mouquet et al., 2012).
(3) Why ‘taxonomic inflation’ is a misnomer
In contrast to the general belief among biologists
and conservation practitioners, our actual knowledge of
large mammal diversity is poor. Taxonomic inertia has
undermined a representative knowledge of ungulate diversity
for far too long. There is disquieting evidence that the
traditional ungulate taxonomy not only rests on remarkably
weak scientific foundations, but also that significant diversity
is still unknown and underexplored. Over decades, these
repeated failures by professionals flow from the artificial
classification of poorly known evolutionarily distinct taxa
into single polytypic ‘species’. The number of genuine
taxonomic revisions that have been conducted on African
ungulates – in fact, on any ungulate genera at all – can be
counted on the fingers of one hand. Moreover, in these
few cases hypodigms were limited, often based on only one
museum’s collection (almost invariably the Natural History
Museum, London). Critically evaluated against this complete
lack of revisionary work, it is clear that the term ‘taxonomic
inflation’ is a misnomer, at least as far as ungulates are
concerned: quite simply, there has been no taxonomy to
be inflated.
Most seriously, many mainstream conservation practition-
ers appear unaware of these realities. Park managers and zoo
directors alike assume that existing knowledge of ungulate
diversity is resolved. Thus no species remain unrecognized;
for surely, give or take adjustments of the ‘subspecies’ status
of a few populations, is it not true that species lists were com-
pleted decades back? Moreover, where their conservation
profile is disregarded as just population segments, subspecies
Biological Reviews (2017) 000– 000 ©2017 Cambridge Philosophical Society
Taxonomic inertia and ungulate conservation 5
Table 1. Summary of over a century of classification of African ungulates revealing significant shifts in recognized species diversity
Family/subfamily
Sclater & Thomas
(18941900)
Lydekker & Blaine
(19131916)
Allen
(1939)
Meester & Setzer
(1971)
Corbet & Hill
(1986)
Grubb
(2005)
Groves & Grubb
(2011)
Rhinocerotidae 2 2 2 2 2 3
Equidae 5 5 5 4 4 5
Suidae 8 5 4 4 6 8
Hippopotamidae — 2 2 2 2 2 3
Tragulidae 1 1 1 1 1 1
Giraffidae 3 3 2 2 2 9
Cervidae 1 1 1 1 1 1
Bovinae 1410 11 10 10 10 39
Cephalophini 20 33 18 16 17 18 41
Reduncini+18 12 10 9 9 9 24
Hippotragini 9 7 7 7 7 8 11
Alcelaphini 18 14 10 7 7 10 25
Aepycerotini 2 1 1 1 1 1 2
Antilopini 39 48 34 27 26 24 60
Caprini 3 3 2 2 3 3
Total number 120 150 113 96 95 101 235
Does not include Syncerus.
+Includes Pelea (following Robinson et al., 2014).
are of negligible evolutionary importance (Corbet, 1997). We
argue that all ‘de facto’ factors such as these have motivated
zoos and wildlife authorities to mix supposedly ‘conspecific’
stocks both in situ and ex situ (but see Dathe, 1978).
Nothing less than a landmark taxonomic revision was
needed to galvanize attention to taxonomic inertia of the
ungulates. The incisive synthesis by Groves & Grubb (2011,
hereafter G&G) compiled revisions carried out through a
collective eight decades of research, within the strictures of
available hypodigms in museums. Remarkably, it has met
with not just surprise, but hostility, in antagonism against
doubling the recognized number of species of ungulates.
Unfortunately, too few critics appear to understand not only
the motivations but especially the empirical foundations
underpinning G&G. One line of criticism seized upon
weaknesses perceived in the PSC used to reclassify the
ungulates. The PSC was used explicitly as a workable proxy
for the ESC. The G&G revision considerably increased
the number of recognized species as highlighted by a
synthesis of how species diversity of African ungulates has
been evaluated over more than a century (Table 1). G&G
finally recognized 235 species of African ungulates after
studying unprecedented hypodigms of specimens (Cotterill
et al., 2014). Although one of the earliest species lists (Lydekker
& Blaine, 19131916) was already influenced by lumping,
it is, nonetheless, interesting to note how its total of 150
species dropped in subsequent years. This finally reached
a minimum with Corbet & Hill (1986) of only 95 African
ungulate species. Interestingly, the number of global primate
species followed a similar trend: decreasing from 532 in 1912
to only 180 in 1967 followed by an increase to 233 in 1993,
370 in 2001, and 480 in 2013 (Rylands & Mittermeier, 2014).
With the application of morphometric and genetic methods,
in combination with the PSC, we have learned more about
primate taxonomy and evolution in the 13 years following
Groves (2001) standard work on primate taxonomy than in
the 50 years preceding Groves’ book.
It is important to acknowledge that G&G is the precursor
and catalyst for much taxonomic work that remains
unfinished. This applies especially where hypodigms are
small, as the high prevalence of incomplete hypodigms
makes the assessments of many populations tentative.
These inadequate samples of populational variation of
many hypodigms of candidate ungulate taxa are a strident
indicator of severe gaps in knowledge of large mammal
diversity – poor representation in the available and/or
examined museum collections (cf . Reddy & D´
avolos, 2003).
For example, no oribi Ourebia sp. from north of the Juba
River, Somalia, generally ascribed to the taxon haggardi,have
been studied and the few existing museum specimens await
comparison against the population from southern Somalia
and coastal Kenya. Wide-ranging species, such as the bongo
Tragelaphus euryceros, are mostly known from old museum
specimens received from a tiny part of their range –despite
this species being nowadays highly prized by trophy hunters
in Central Africa. Sample sizes are invariably small and the
last original taxonomic work dates from the beginning of
the 20th century (Thomas, 1902). In a little-known paper on
the African buffalo in southern Somalia, Fagotto (1980)
reported the existence of two ‘types’; one lightly built,
with horns which never curve downwards below the
level of the skull base and resembling the taxon Syncerus
brachyceros, while the more massive form with horns that
curve considerably downwards points to affinities with
S. caffer. Interestingly, this latter form is present from the
borders with Kenya to the lower Sheebeli River (Awai),
beyond which the lighter form predominates northwards
along the Sheebeli lower course. The small amount of
material available in Italian museums is not likely to
help us solve this taxonomic question. Similar cases are
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6S. Gippoliti and others
certainly widespread but, belatedly, G&G have unlocked a
new scientific era in large-mammal taxonomy. Important
collections in southern African museums, especially the
rich collections in the Natural History Museum, Bulawayo
(NMZB), have yet to be comprehensively evaluated,
with the exception of Damaliscus lunatus and Kobus leche
species complexes studied by Cotterill (2003a,b, 2005) and
unpublished results on Kobus cf. vardoni and Hippotragus
(F. P. D. Cotterill, unpublished data). This Bulawayo
collection is complemented by significant large mammal
collections in Pretoria (TM, Ditsong Museum), East London
(Amathole Museum), Cape Town (SAM, Izoko Museum)
and Zambia (Livingstone Museum), and smaller but still
significant collections in the Kenya National Museum,
Nairobi, and the Institut Fondamental d’Afrique Noire
(IFAN), Dakar. Regrettably, it seems that the importance
of a national repository for natural history collections is
not receiving attention in several African countries. There
are ample possibilities for European museum collections to
contribute to taxonomic studies (e.g. D’Huart & Grubb,
2001; Gippoliti et al., 2014) but this requires a paradigm shift
in current perceptions of natural history museums and their
collections (Cotterill, 2016).
Finally, apart from the vast amount of morphological
data stored in museum collections, molecular studies offer
an opportunity to uncover much of the geographical and
temporal genetic variation held there. However, genetic
studies of historical museum specimens typically rely on
extracting highly degraded and chemically modified DNA
samples from skins, skulls or other dried samples. Until
recently, it was possible only to obtain short fragments of
DNA sequences using traditional polymerase chain reaction
(PCR) amplification. Recently, however, approaches using
high-throughput next-generation sequencing to obtain
reliable genome-scale sequence data have been proposed
(e.g. Rowe et al., 2011). This allows obtaining data
for single-nucleotide polymorphisms (SNPs) or complete
mitochondrial genome sequences even from degraded
source materials. The biological material required can
be as little as 10 mg with high success rates of PCR
amplification. This is particularly important when sampling
from museum specimens, as it avoids destructive tooth
or bone sampling (Wandeler, Hoeck & Keller, 2007;
Guschanski et al., 2013; see also Bi et al., 2013). Museum
collections allow genotyping of type specimens, as was
recently carried out for the lectotype of the Arabian gazelle
Gazella arabica consisting of a skull and skin, which led
to the discovery that it was of composite origin and only
the skin should be retained as the name-bearing specimen
(B¨
armann et al., 2013). Obviously it is now possible to sample
museum specimens belonging to extinct taxa/populations
to produce more-complete phylogeographic information
to resolve taxonomic issues concerning highly threatened
species. This has been done with the Nubian wild
ass Equus africanus (Kimura et al., 2010) and the
giant sable antelope Hippotragus niger variani (Themudo,
Rufino & Campos, 2015).
III. TAXONOMIC INFLATION AND
CONSERVATION
Several prominent conservation geneticists who have
invested decades of research efforts to the identification and
conservation of distinctive and often-threatened evolutionary
units (e.g. Frankham et al., 2012; Heller et al., 2013, 2014;
Zachos et al., 2013a,b) are strongly opposed to the shift in
mammal taxonomy resulting from adoption of the PSC
(Groves, 2001; Groves & Grubb, 2011). The rationale
underlying this criticism lies in concerns over dissipation of
conservation resources on populations traditionally lumped
into single ‘species’, using the BSC. Such opposition is
ironic given the contributions of these and other geneticists
to the uncovering of discrete lineages within traditionally
recognized species.
Underlying this criticism is the argument of Isaac et al.
(2004) that excessive taxonomic splitting impacts negatively
on macroecological research and conservation. First, we
should note that part of their problem lies in the current
biased application of ESC in mammalogy. At present we
have an ESC synthesis for Primates, Artiodactyla and
Perissodactyla while other orders, such as Hyracoidea,
remain classified in an overlumped BSC-based taxonomy.
This problem is attributed to the present period of transition,
not an underlying flaw within the ESC itself.
Regarding the supposed negative effects of a PSC-based
taxonomy, we note that a survey by Morrison et al. (2009)
found no evidence for negative effects of taxonomic splitting
on conservation, but rather found the exact opposite: in
addition we highlight the dubious record of ‘orthodox’
taxonomy in creating long-standing ex situ problems, e.g. in
zoo breeding programs during the 20th century. Here the
legacy of ‘taxonomic inertia’ is manifested by overlooking
finer scale diversity and the geographical origins of founder
populations, bequeathing chimerical stocks of zoo ungulates
of unknown and/or admixed evolutionary lineages. As a
potpourri of different populations, the ex situ conservation
status of these purported ‘species’ is disputable. For example,
two supposed subspecies of East African dikdik Madoqua
kirkii had different karyotypes and were found to produce
infertile offspring when interbred in zoos (Kumamoto,
Kingswood & Hugo, 1994; Cernohorska et al., 2011); there
are in fact four species, morphometrically distinguishable,
within what was lumped as M. kirkii, and skulls of dikdik
of known karyotype could easily be identified by being
fitted in to this scheme (Groves & Grubb, 2011). A study
of the karyotypes of the North American zoo population
of suni Nesotragus moschatus found even greater chromosome
variability, with Kenyan animals (N. m. akeleyi) exhibiting
2N =56 and KwaZulu-Natal animals (N. m. zuluensis)2N
=52 (Kingswood et al., 1998). It was sensibly suggested that
these two ‘subspecies’ should be managed separately given
evidence of probable breeding problems in hybrids, and they
are now classified as different species by G&G. In another
study, heterozygosis for three chromosomal changes (centric
fusions) was invoked as causing high perinatal mortality in
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Taxonomic inertia and ungulate conservation 7
captive Soemmering’s gazelles Gazella soemmeringi (now Nanger
soemmerringii) (Benirshke et al., 1984), although, in this case, it
is unclear whether chromosomal rearrangements correlate
with subspecific status and thus what the possible roles of
inbreeding and outbreeding in perinatal mortality might be
(see Steiner et al., 2016, who suggested a genetic and chro-
mosomal study of wild populations to clarify the relationship
between taxonomic status and chromosomal rearrangements
in Soemmering’s gazelles). There are at present not many
captive breeding programmes for small and medium-sized
ruminants representing the Antilopini, Cephalophini and
Tragulidae; so opportunities comprehensively to evaluate
effects of outbreeding remain severely limited. Nonetheless,
available data suggest that the karyotypic diversity of the
Bovidae is more similar to that of rodents than to other
large mammals such as carnivores (Kumamoto et al., 1999;
Pagacova et al., 2011; Robinson & Ropiquet, 2011).
Outbreeding depression (Storfer, 1999) is now recognized
to be as great a problem as inbreeding depression in wildlife
conservation and captive breeding programmes. Its negative
effects persist even after admixture of distant populations
of apparently monotypic species such as Arabian oryx Oryx
leucoryx (Marshall & Spalton, 2000). Pedigree analysis has
revealed outbreeding depression in captive populations of
Indian rhinoceros Rhinoceros unicornis representing separate
populations from Nepal and Assam (Zschokke & Baur,
2002); belatedly, these two genetically distinctive populations
are now acknowledged to be best managed separately
(Zschokke et al., 2011). Although similar cases of breeding
incompatibility likely exist in several other rhinoceros
populations in Africa and Asia, their classification as
‘subspecies’ confers a dubious status on these populations.
This is most notorious when ‘just a subspecies’ is declared
extinct (Gippoliti et al., 2013). This is the case of the Nile
rhinoceros (northern white rhinoceros) Ceratotherium cottoni,
of which only three individuals are still living in captivity
and apparently none in the wild. The species rank accorded
by Groves, Fernando & Robovsk´y (2010) has been recently
challenged by Harley et al. (2016) fearing that the rescue
and conservation of C. cottoni through hybridization with
the southern white rhinoceros C. simus may be prevented
by taxonomic splitting; yet there is strong evidence that the
only female hybrid produced in Dvur Kralove Zoo showed
signs of outbreeding depression, never bred and was larger
and heavier than any other recorded female (Dvur Kralove
Zoo records). As evidenced by a recent proposal to manage
Sumatran and Bornean rhinoceros Dicerorhinus sumatrensis
as a single ‘management unit’ (Goossens et al., 2013), some
conservationists continue the dubious practice of overlooking
negative consequences of outbreeding depression. Note,
however, that the absence of any perceived negative effect
from introgression of two or more closely related taxa does
not constitute a criterion for their conspecificity.
The species of African ungulates rated as extinct or
near-extinct over the last two centuries makes sobering
reading (Table 2). Although the taxonomic status of
some of these taxa is still controversial, biogeographical,
morphological, and genetic evidence (where known)
suggests that these extinctions have extirpated considerable
phylogenetic diversity. Orthodox taxonomy stands out as
the propagator of several extinctions, especially in the past
half a century. Conspicuous losses of phylogenetic diversity
among wide-ranging African mammals are exemplified by
the black rhinoceros Diceros spp. (Moodley et al., 2017).
The distinctively long-legged black rhino Diceros longipes
from the Chad region presently recognised as Diceros
bicornis longipes would certainly have received much greater
attention and conservation support had its morphological
and taxonomic distinctiveness been thoroughly investigated.
Furthermore, given the high value people place on rarity
(Angulo et al., 2009), this species should have constituted an
exceptional flagship species for conservation in west-central
Africa, and an important focus for tourist attraction in a
region otherwise neglected.
The case of the Nubian wild ass Equus africanus stands
unique among all these extinctions. It was treated as one of
at least two subspecies (the other being the Somali wild ass
Equus somaliensis; see Groves & Smeenk, 2007 for a recent
synthesis), until the distinction of these lineages was confuted
after the mid 20th century. As a result the Nubian wild ass
practically disappeared from the scientific and conservation
literature (Gippoliti, 2014). Recent genetic studies seeking
to resolve the origin of donkeys Equus asinus genotyped old
museum specimens. These confirm the distinctiveness of
the two taxa, highlighting the Nubian wild ass as ancestor
of the donkey (Kimura et al., 2010); it is perhaps not too
late to save this neglected species from extinction, as there
are at least a few individuals, now carefully protected,
persisting in south-eastern Egypt (Sultan Mos’ad, personal
communication).
IV. TRANSLOCATION ‘RESCUE’ AND
CONSERVATION GENETICS
Several critics of the PSC argue that small and declining
populations might be rescued through translocations from
other populations, but such conservation ‘rescue’ efforts are
undermined now that these populations are characterized
as distinct (Frankham et al., 2012; Zachos et al., 2013b;
Heller et al., 2014). Besides the failure to find concrete
examples to support this fear of a (theoretical) conservation
hurdle, this argument overlooks the respective evolutionary
histories of populations lumped into single ‘species’, and runs
counter to the increasing role of phylogenetic knowledge
in informing conservation decisions. Moreover, the findings
of Heller, Okello & Siegismund (2010), on genetic drift
in Syncerus caffer, confined in isolated protected areas of
Uganda and Kenya, clearly show that human-mediated
gene flow can be pursued without breaking the deeper
phylogenetic barrier that has evolved along the Victoria Nile.
On the contrary, we know of a few cases of ecological and
behavioural disruptions following mixing of evolutionarily
divergent lineages. In a classic case, the translocation of
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8S. Gippoliti and others
Table 2. Extinct and near-extinct African ungulates in recent history
Taxon English name Original range Notes
Dicerosbicornislongipes
Western black rhinoceros Nigeria, Cameroon, Central African
Republic (CAR)
Extinct 2012
Ceratotherium cottoniNile rhinoceros W. Uganda, S. Sudan, Garamba NP
(Democratic Republic of Congo),
CAR, Chad
Three individuals of breeding age in
semi-captivity
Equus quagga quaggaQuagga S and E Cape, Free State (S. Africa) Extinct 1872
Equus africanusNubian wild ass N Eritrea, NE Sudan, SE Egypt Status uncertain, Gebel Elba, Egypt
and possibly in Sudan
Phacocoerus aethiopicusCape warthog S. Cape (S. Africa) Extinct
Choeropsis heslopiNigerian pygmy
hippopotamus
Niger Delta, Nigeria Probably extinct
Giraffa camelopardalisNubian giraffe NW Kenya, Ethiopia, Eritrea, Uganda,
Sudan (E of Nile)
Survives patchily in Kenya, Uganda,
Sudan, far-western Ethiopia
Kobus robertsiRoberts’ lechwe NE Zambia Extinct by 1950s
Hippotragus leucophaeus Blaubok SW Cape, Free StateExtinct 1800 (1860 if Free State record
is valid)
Alcelaphus buselaphusBubal hartebeest North Africa Extinct 1925
Alcelaphus toraTora hartebeest Nubia and W Ethiopia Possibly extinct 2010
Damaliscus selousiSelous’ topi Uasin-Gishu plateau, Karamoja Extinct sometime after 1930
Eudorcas rufina Red gazelle Algeria Extinct pre-1894
Denotes taxa not included in Turvey (2009).
This information comes from a claim of an eyewitness report of what sounds like blaubok in the Free State, in 1858. See Groves & Grubb
(2011, p. 198).
three interbreeding members of the genus Capra (Capra
ibex,C. nubiana and C. aegagrus, the latter two at that time
considered subspecies of C. ibex) on the Tatra Mountains
failed because of a different birth seasonality (Templeton,
1986). Geist, O’Gara & Hoffmann (2000) discussed how
wapiti and European red deer (Cervus canadensis and Cervus
elaphus species complexes) differ in their respective habitat
requirements and behavioural ecology, suggesting that
interbreeding can be advantageous only in semi-captive
situations. Such cases imply that the concern expressed by
several researchers (Frankham et al., 2012; Heller et al., 2013;
Zachos et al., 2013a,b) over the conservation consequences
of adopting the PSC is misplaced and unwarranted.
Paradoxically, wealthier African countries, such as South
Africa, face the biggest problems in protecting their original
ungulate diversity due to a mix of liberalism in wildlife
management and unsound use of scientific knowledge;
taxonomic inertia apparently plays a role. It is true that
modern conservation biology recognizes the importance of
maintaining intraspecific diversity [evolutionarily significant
units (ESUs), management units (MUs), subspecies] (Moritz,
1994; Crandall et al., 2000), yet such detailed attention is
often accorded only to a few species in particular regions,
mostly in North America or Australia (Haig et al., 2006;
Gippoliti & Amori, 2007). Most national legislations protect
species, and species are the mandatory focus of IUCN Red
List assessments (see www.iucnredlist.org). Identification of
biodiversity hotspots or sub-hotspots is based on endemic
species distributions, not on the distribution of subspecies
or ESUs (Dubois, 2003). In the few cases where resources
are abundant, due attention should be paid to intraspecific
variability (e.g. lion Panthera leo;tigerPanthera tigris; gorilla
Gorilla spp.; Wilting et al., 2015; Bertola et al., 2016) but this is
the exception rather the rule. Even highly charismatic large
mammals receive very little attention from this point of view
(e.g. African elephant Loxodonta spp.; brown bear Ursus arctos:
see Gippoliti, 2016; Groves et al., 2016). The zoo community
has so far allowed the mixing of Sumatran and Bornean
elephants within continental Asian family groups, despite the
strong phylogeographic structure found in Elephas maximus
(S. Gippoliti, personal observation).
Although South Africa should urgently adopt new
regulations to limit ecological and genetic effects of ungulate
translocations in private reserves (Cousins, Sadler & Evans,
2010) with the aim of avoiding further negative consequences
for native biodiversity, this still seems far from being achieved.
Yet, adoption of an ESC-based taxonomy would be a
step in the right direction. For example, the only buffalo
native to South Africa remains Syncerus caffer, but the G&G
taxonomy restricts this species to the southern and eastern
African savannahs east of the Western Rift Valley, while
Central and Western buffaloes are recognised as belonging
to three distinct species (S. brachyceros,S. mathewsi and S.
nanus) and, as exotic species, their importation could be
easily regulated or even prevented. Unregulated wildlife
translocations had severe consequences in North America
and Europe (Champagnon et al., 2012), and we may easily
imagine negative impacts among ungulates in Africa.
In some cases translocations of rare ungulates become
cosmetic initiatives at best; this is the case for ‘sitatunga’
(Tragelaphus spekii complex) reintroduction in The Gambia.
In fact, the sitatungas west of the Dahomey Gap seem to
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Taxonomic inertia and ungulate conservation 9
represent an undescribed, very-little-known potential species,
but apparently no data are available on the origin of
the four individuals released at Abuko in 1968 (Starin,
2000). The fact is that one consequence of taxonomic
inertia is that of dismissing the role of the whole discipline
of morphology-based taxonomy, which some believe is
superseded by phylogeographic molecular studies.
Transmission of new diseases or failure to acclimatize
to endemic diseases is another widespread problem
encountered in the management of translocated ungulate
populations (Melter, 1993; Nijhof et al., 2005), and often
neglected by population geneticists. Interestingly, Nijhof et al.
(2005) reported the case of a pair of roan antelope Hippotragus
equinus originating from Togo and Benin succumbing to a
Theilerosis infection after release on a game ranch in southern
Mpumalanga, South Africa. As Aiello et al. (2014) showed
with the desert tortoise Gopherus agassizii, translocations and
augmentation may disrupt existing resident disease dynamics
and initiate an outbreak that would effectively offset any
advantages accompanying the translocation.
The dramatic recovery of the (southern) white rhinoceros
Ceratotherium simum in Kwazulu-Natal [but see Rookmaaker
(2000) for a critical review of historical data] shows that
the paradigm of population genetic theory (see Caughley,
1994) has been overemphasized in conservation biology at
the expense of factors such as political stability and effective
management and protection. If this is true, the current
emphasis on gene flow and human-mediated translocations
in ungulate conservation needs to be considered in a wider
perspective.
V. THE ROLE OF HYBRIDIZATION IN SPECIES
CONCEPTS AND CONSERVATION
In the past, interbreeding or hybridization between animal
species was assumed to be of negligible concern, not at
least because of a near-universal belief in the infallibility
of the BSC as the conceptual tool with which taxonomists
classified living diversity; thus fertile interbreeding taxa by
definition were regarded as belonging to a single species.
Thanks to progress in molecular methods over the last
decades, however, it has become obvious that gene flow
between species has been widespread in the past, and
continues in the present, in various taxonomic groups (e.g.
Mallet, 2005; Arnold, 2008; Schwenk, Brede & Streit, 2008;
Zinner, Arnold & Roos, 2011). Following in the footsteps
of botanists, there is increasing interest among zoologists in
the role of hybridization and its evolutionary consequences,
ranging from zero gene flow when F1 individuals are sterile
to complete admixture or hybrid speciation (Arnold, 1997;
Allendorf et al., 2001; Larsen, March´
an-Rivadeneira &
Baker, 2010; Abbott et al., 2013). Given that species delimita-
tion is not a simple endeavour, not least because no universal
definition of species is yet accepted, despite the arguments of
de Queiroz (2007) and others, gene flow among taxa makes it
even more complicated. Hybridization can have significant
conservation impacts, in particular when conservation
is species-based (Simberloff, 1996; Allendorf et al., 2001;
Fitzpatrick et al., 2015; van Wyk et al., 2017). Questions arise
about the worthiness for conservation of populations with
hybrid ancestry, with inherent problems in the legal treat-
ment of hybrid populations (Fitzpatrick et al., 2015; Richards
& Hobbs, 2015). Often a distinction is made between
‘natural’ and ‘human-caused’ hybridization, although in
many cases it remains unclear what proportion of contem-
porary hybridization can actually be attributed to direct
(e.g. purposely introduced species) or indirect (e.g. species
range expansion due to human-caused habitat alterations or
climate change) human activities (Mallet, 2005).
Molecular techniques can detect past introgressions that
shaped the evolutionary histories of lineages (Zinner, Arnold
& Roos, 2009; Green et al., 2010), yet such events have
not always been suspected on morphological grounds (but
see Ackermann & Bishop, 2010; Ackermann et al., 2010).
Accumulating evidence of gene flow between both universally
recognized species, even of different genera [e.g. in primates
(Roos et al., 2011; Zinner et al., 2011); in bovids (Verkaar et al.,
2004; Rodríguez et al., 2009)], as well as between ‘subspecies’,
undermines the roots of the BSC with its emphasis on
reproductive isolation (Mallet, 2008). This evidence for
interspecific gene flow makes it all the more difficult to
single out what qualifies as a true species, and why such
populations differ from those that comprise a hybrid swarm,
as Ruxton & Schwarz (1929) proposed decades earlier for
East African Alcelaphus.
After studying two specimens of hartebeests from
south-west Ethiopia, de Beaux (1943) proposed that, when
a hybrid population shows constant characters, it should be
recognized as a distinct taxonomic entity. In this specific case,
he proposed that Alcelaphus buselaphus neumanni (Rothschild)
should be accepted with the following synonymy: ‘Alcelaphus
buselaphus lelwel (Heuglin) ×Alcelaphus buselaphus tora (Gray)
Ruxton and Schwarz’. More recently, Ouma et al. (2011)
investigated the genetic status of putative hartebeest hybrids
in Kenya. With respect to the declining status of these
populations, they affirmed that ... in many African
countries, including Kenya, where there has been little
mixing of populations by translocation, opportunities to
conserve ongoing evolutionary processes persist, and should
be pursued’ (Ouma et al., 2011, p. 146). A proposed hybrid
swarm from divergent caribou lineages (Rangifer tarandus
tarandus and R. tarandus caribou) is considered a conservation
target in Canada (McDevitt et al., 2009). These examples,
both old and recent, highlight the need to reconsider
the taxonomic and conservation implications when we
acknowledge that hybridization is an historical process.
Moreover, much greater attention should be paid to the
possible detrimental effects of wildlife translocations or the
further reduction of sympatric populations of closely related
taxa that may encounter increased incidence of hybridization
due to the absence of conspecific mates. Paradoxically,
ungulate managers have often had privileged opportunities
to study artificially introgressed populations, yet the
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10 S. Gippoliti and others
intricacies of natural evolutionary trajectories receive little
attention.
The complexity of conservation in cases of hybridization
becomes clear where human activities induce introgression
directly or indirectly, as summarized above (see also
Allendorf et al., 2001). The intentional or unintentional
introduction of closely related non-indigenous species may
lead to hybridization. Similarly, reduced population sizes
of related sympatric or parapatric species (through hunting
or other human impacts), might increase hybridization risk,
eventually leading to the extinction of one or both species
(Frankham, Ballou & Briscoe, 2002; Allendorf, Luikart
& Aitken, 2012; Fitzpatrick et al., 2015). In South Africa
there has been considerable concern about introgression of
southern blue wildebeest Connochaetes taurinus genes into the
local endemic black wildebeest Connochaetes gnou following
inopportune introductions of the former species into the
latter’s range (Grobler et al., 2011). But many more taxa
seem affected; some cases have been discussed in detail,
such as hybridizations between greater kudu and lowland
nyala Strepsiceros strepsiceros ×Tragelaphus angasi,orred
hartebeest and tsessebe Alcelaphus buselaphus ×Damaliscus
lunatus (Robinson et al., 2015). Furthermore, admixtured
populations of the Karoo and Kalahari springbok (Antidorcas
spp.) are purposely farmed for venison and trophy hunting
(Van Aswegen, Labuschagne & Grobler, 2012). Zebras
are also potentially affected by translocations in South
Africa (Castley, Boshoff & Kerley, 2001), with potentially
devastating effects for the now-recognized species Cape
mountain zebra Equus zebra and Hartmann’s zebra Equus
hartmannae. Introduction of scimitar-horned oryx Oryx dammah
into the historic range of gemsbok Oryx gazella puts the genetic
integrity of the latter at obvious risk (Castley et al., 2001).
Similarly, black-faced impalas Aepyceros petersi are also affected
by unregulated translocations (Green & Rothstein, 1998).
Introgression over the long term may reduce the abilities
of such species to adapt to present and future environmental
change (Rhymer & Simberloff, 1996) or may lead directly
to cytonuclear extinction (e.g. Gill, 1997; Cordingley et al.,
2009). So whether such evolutionarily distinct lineages
are termed species, ‘subspecies’, ESUs (Ryder, 1986), or
‘ecotypes’ (and so on), it is mandatory that we manage such
phylogenetically distinct lineages separately. In summary, the
negative impacts of outbreeding depression or introgression
underscore how the ESC (=PSC) derived taxonomy of
ungulates provides wide-ranging epistemological support to
biodiversity conservation. That this is evidently not the
current situation is clear from the widespread criticism of
G&G when they raised some subspecies to species rank.
VI. HOW CAN A ‘NEW ALPHA TAXONOMY’
SUPPORT CONSERVATION?
(1) Forgotten taxa, forgotten hotspots
Recent revisions of East African giraffes reveal that the
three recognized species are confined to discrete ecoregions,
within which synchronization of birth season with rainfall
may be one mechanism that reduces gene flow among giraffe
species (Thomassen et al., 2013). Belated recognition of the
real diversity of Giraffa (Brown et al., 2007; Groves & Grubb,
2011; Bock et al., 2014) exemplifies how the taxonomy of
these large mammals provides a framework to explore such
processes, provided it is founded on a lineage species concept.
The new alpha taxonomy of the ungulates provides essential
conservation support by highlighting biodiversity hotspots
previously overlooked, such as Katanga, the Zambezi and
the Nile watersheds (Gippoliti et al., 2013; Cotterill et al.,
2014). Equally, it is important to analyse responses of
African large mammals to climate change at the level of
phylogeographic lineages rather than orthodox ‘species’,
since this level of taxonomic precision is a prerequisite
to parse the focal variable in robust models (D’Amen,
Zimmermann & Pearman, 2013).
Although the increase in recognized alpha diversity of
clades might make ‘species conservation’ appear more
challenging to implement, this is vastly preferable to
the converse impacts of imprecise taxonomy fostered by
taxonomic inertia. An example of such impacts are species
allowed to slip into extinction unnoticed; such as the Tora
hartebeest Alcelaphus tora (Heckel et al., 2008), because it was
lumped as one of several subspecies of Alcelaphus buselaphus.
Taxonomic inertia has likewise conferred the dubious
distinction of complete, or near, extinction on such species
as the Nigerian pygmy hippopotamus Choeropsis heslopi,the
Queen of Sheba’s gazelle Gazella bilkis, the Nubian giraffe
Giraffa camelopardalis and the Nile rhinoceros Ceratotherium
cottoni. Arguably, their conservation status today could have
been vastly different had they been accorded species status,
or at least had their status openly debated. The same could be
said of species in imminent danger of following their slide to
extinction. Examples include the West African giraffe Giraffa
peralta, the Arava gazelle Gazella acaciae, the Upemba lechwe
Kobus anselli, and the Mt. Elgon red duiker Cephalophus fosteri.
(2) Taxonomic impacts on the wildlife industry and
sustainable conservation
African wild ungulates are worth many hundreds of millions
of US dollars as a source of protein for rural communities,
as hunting trophies, and as focal subjects of tourist attention
(Yasuoka, 2006; Lindsey, Roulet & Romanach, 2007; Nasi,
Taber & Van Vliet, 2011). Wild ungulates represent the
most notable component of bushmeat consumed in most
areas of the humid forest as well as the Zambezian savannahs
(Newing, 2001; Fusari & Carpaneto, 2006), and an important
source of income for alleviating poverty in rural communities
(de Merode, Homewood & Cowlishaw, 2004). Ironically we
know very little about the enduring escalating impacts of
bushmeat and other depredations on the true diversity of
ungulates. Local mismanagement is encouraged by orthodox
taxonomy, as exemplified by the report into the decline of
blue duiker on Bioko Island (Grande-Vega et al., 2016).
According to G&G, the Bioko island blue duiker represents
an endemic species Philantomba melanorheus (Gray, 1846), but
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Taxonomic inertia and ungulate conservation 11
Grande-Vega et al. (2016, p. 49) claimed that ‘The blue duiker
(Philantomba monticola) is an abundant and widely distributed
ungulate in continental sub-Saharan Africa’. Later they
emphasized that island populations may be more threatened
than others, but never used the name melanorheus in their
paper, even as a subspecific name. This is very different
from the attention paid to the endemic primate assemblage
of Bioko Island, with the fate of seven species/subspecies a
cause of great concern (Butynski, De Jong & Hearn, 2009).
Furthermore, recently, Sarasa (2013) highlighted that
previous analyses evaluating trophy prices and the
international hunting market are confounded by bias because
they overlooked intraspecific diversity of ‘traditional species’.
For example, among Spanish ibex, trophy prices for Capra
pyrenaica victoriae are much higher than Capra pyrenaica hispanica
because the latter has shorter horns. The different IUCN
conservation status of these two subspecies underscores why
the ‘biological species’ taxonomy undermines the accuracy
of comparative studies and conservation assessments.
We highlight the impact of taxonomic inertia on
the classification and equally on the conservation and
management not only of ungulates but also other
charismatic African mega-herbivores, elephants of the
genus Loxodonta. Recognition of the true diversity of this
mega-herbivore obscures the high-profile concern over the
plight of the African elephant, traditionally classified during
the period of taxonomic inertia as a single species. The reality
is that there are two lineages of unequivocal evolutionary
distinctiveness, often recognised by those working first-hand
on the issue (Frade, 1931; Allen, 1936; Azzaroli, 1966).
This is not surprising, given that the genomic evidence
dates the divergence between savanna elephant Loxodonta
africana and forest elephant L. cyclotis to the Pliocene
(Rohland et al., 2010; Roca et al., 2015); crucially, it is L.
cyclotis that is most at risk from unsustainable anthropogenic
depredations, caused by habitat losses and poaching (Maisels
et al., 2013), but taxonomic inertia continues to obscure
its conservation plight. Ironically, morphological revisions
conclusively demonstrated the distinctiveness of the two
species nearly two decades ago (Grubb et al., 2000; Rohland
et al., 2010; Shetty & Vidya, 2011).
The role of African ungulates in the maintenance of
ecosystems, thus contributing ecosystem services to the
value of many millions, even billions of dollars, has only
begun to be estimated. The collapse of large mammal
populations in Central African forests following overhunting
for bushmeat may have long-term consequences for the
ecological integrity of the region (Abernethy et al., 2013).
Activities such as deforestation and hunting have direct
and indirect detrimental effects on ungulate biodiversity
in Africa, and a sound knowledge of alpha taxonomy is
asine qua non successfully to manage, conserve and study
this irreplaceable resource. Pre-G&G taxonomy set a poor
foundation that has misinformed and misled sustainable
management in too many cases. We have highlighted many
conspicuous failures in which the extreme tragedy – species
extinction has occurred repeatedly. In the case of large
mammals, an outdated phenetic approach goes a long way to
explain this ‘domino-impact’ of weak science on conservation
policy and applied management (Cotterill et al., 2014).
We single out the persistence of a spurious alpha
taxonomy as the cause of biotic homogenization across
large regions of Africa, in the way that in some countries,
such as South Africa, translocations of various exotic or
extralimital ungulates is now considered a major risk to native
biodiversity (Castley et al., 2001; Spear & Chown, 2009), and
hybridization has seriously affected some threatened species
such as Connochaetes gnou and Damaliscus pygargus (van der Walt,
Nel & Hoelzel, 2013).
(3) How precise and accurate taxonomy informs a
hierarchical conservation strategy
A persistent challenge in conservation is to reconcile the
often disparate goals and challenges of single-species versus
ecosystem management, where the latter aims to maximize
biodiversity conservation. Ultimately, any single-species
conservation will fail in situ where ecosystem integrity is
ignored. This is where we highlight the increasing use in
conservation biology of decision-making processes relying on
phylogenetic diversity (PD) to identify and rank conservation
areas. It is no accident that the evolutionary lineage is the core
currency of PD calculation to diagnose biodiversity hotspots
and evolutionarily vibrant landscapes [as first argued by
Erwin (1991) and see Mouquet et al. (2012)]. This approach
should ideally utilize both ancient and young lineages in
combination to map the most complete (i.e. representative)
range of unique landscape elements across the continent.
In the case of Africa, there have been major attempts
to identify biogeographical patterns using indicators of
evolutionary history of representative biota (e.g. Linder et al.,
2012), but the lack of primary information still weakens
this quest. G&G present a strong data set, where their
classified evolutionary species can be mapped out in the
most complete detail that locality data permit currently.
The strength of this approach is exemplified by Moodley
& Bruford (2007) who integrated occurrence maps of the
lineages of the Tragelaphus scriptus and T. sylvaticus species
complexes into the matrix of African ecoregions. These
lineages of African bushbucks are demonstrated to provide an
informative proxy of palaeoecological affinities, and at a finer
scale a recent evaluation of endangered okapi (Okapia johnstoni)
reveals equally instructive evidence linking taxonomy to
ecoregions, especially where respective okapi lineages exhibit
congruence with other species (Stanton et al., 2014). Ironically
today, these ungulates diagnose high conservation values of
landscapes in which some indicator lineages appear to have
been extirpated.
Much work remains. We single out this evolutionary con-
servation strategy [the PD strategy] as a significant – if not
the primary practical strength of an ESC-based taxon-
omy in biodiversity conservation. Following King (2009),
application of the PSC at the population level minimizes
taxonomic errors, pertinently in applications informing in
situ planning and policy. At the ecosystem/landscape level,
Biological Reviews (2017) 000– 000 ©2017 Cambridge Philosophical Society
12 S. Gippoliti and others
ungulates rank as textbook flagship/umbrella species, and as
especially informative indicators, where their evolutionary
histories can inform biodiversity maps, and in turn diagnose
biodiversity hotspots. Indeed, G&G emphasize this in their
Introduction (G&G, p. 17) where they flag some of the main
ecosystems revealed by local endemics of ungulates.
VII. CONCLUSIONS
(1) Science informs conservation, not the other way round.
In this respect, it is unfortunate that only within the past seven
years have conservation decision-makers been able to exploit
a sufficiently accurate and precise taxonomy of ungulate
diversity.
(2) In its role in revising biodiversity mapping, the new
taxonomy complements biogeographical data sets of other
indicators (pertinently the herpetofauna and avifauna), but
these data are still incomplete, and/or await electronic
databasing.
(3) Several salient lessons explain why the revision by G&G
has revealed so many new, and significant, findings, issues,
and challenges for ungulate conservation.
(a) It highlights the application of modern taxonomic
methodology whereby high-quality knowledge feeds
conservation policy. This is notable where the identification
of hitherto-unrecognised evolutionary species at the same
time identifies overlooked conservation areas (e.g. Upemba
Swamps).
(b) Taxonomic assessments remain impossible without
tentelic records preserved in museums, especially as
the primary data of conservation concern are open to
independent checks, and focal studies, particularly using
new molecular methods.
(c) The largest data set ever assembled for ungulates
underscores the primacy of a specimen-based taxonomy
over ‘expert’ opinions/assumptions. It is urgent that
collecting of specimens such as hunting trophies, bushmeat,
cropping exercises and pick-up specimens (e.g. road-killed
and predator-killed animals) becomes the norm, where
feasible in conservation terms, facilitated by government
and conservation authorities. Ultimately, we should aim to
collate and utilize all available material in world collections
to fill gaps in taxonomic knowledge that can in turn be
translated into conservation strategies.
(d) Integration of morphology-based taxonomy has the
further merit of being potentially ‘palatable’ to exploiters
such as wildlife tourists (or indeed trophy hunters), and
serves as a vital mechanism to provide DNA to systematists
whose revisions are challenged by gaps in representation of
populations and/or geographical locations.
(e) As argued elsewhere at length (Cotterill et al., 2014)
these tentelic data that vouch for the data analysed in G&G
were classified employing modern methods of phylogenetic
systematics, and not least a species concept that replaces
the polytypic BSC with the lineage-based ESC (=GLC)
operationalized by the PSC. In short, G&G integrate
the complementary strengths of population-thinking and
tree-thinking.
(f) Contrary to Frankham et al. (2012), adoption of the
PSC has highly positive rather than negative consequences
for conservation science, especially in its characterization of
allopatric diversity.
(g) With improvements in precision and accuracy
(minimizing Type 2 and Type 3 taxonomic errors), G&G
sets the precedent to incorporate its classified lineages
into conservation-focused databases that integrate measures
of phylogenetic diversity to inform policy, especially in
implementing the Convention on Biological Diversity at
national, regional and global scales.
VIII. ACKNOWLEDGEMENTS
We thank Christian Roos, Giovanni Amori and Ernesto
Capanna for valuable discussions on earlier versions of the
paper. We also thank Eva B¨
armann and two anonymous
referees who identified weaknesses and helped to strengthen
the paper.
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... Wildlife managers, like most tourists, are convinced that our knowledge of large African mammals is more than satisfactory, as demonstrated from the large number of books existing on the subject e.g., [38,39]. Field guides, in particular, are suspected to vehicle an assuring view concerning our taxonomic knowledge of mammals [40]. Most users are unaware that such tools as field guides are intended to help identify what people see in a given place (i.e., to distinguish a bushbuck, Tragelaphus scriptus (Pallas, 1766) from a sitatunga T. spekii Speke, 1863; taxonomy follows predominantly [41]) but say nothing about the number of taxa, their phyletic relationships, and the rank accorded inside the sitatunga and the bushbuck concepts [42]. ...
... Ironically, translocations may also be responsible for the extinction of pure genetic lineages via hybridization, thereby negatively impacting endangered, indigenous, and rare species. Owing to a general neglect of taxonomy-following the so-called "taxonomic inertia" period described by [40]-it is highly probable that the hybridization problem is greatly undervalued in conservation circles. However, a more subtle danger is the general distortions of the genetic landscape, especially of wild ungulates, as is often reported in North America and Europe [85] but also from Africa [86], which may preclude further research, and which may create management problems that cannot be properly anticipated. ...
... Recently, an important contribution came from [98], which also included genetic data from key museum specimens belonging to now extinct populations. Among the most important findings include the description of a new-historically extinct-taxon from Senegal, G. camelopardalis senegalensis Petzold, Magnant, and Hassanin, 2020, which went extinct around 1970; the revalidation of G. g. wardi Lydekker, 1904; and a stricter geographical delimitation of the nominal G. c. camelopardalis, which make this taxon, the Nubian giraffe, another example of a taxon "allowed to slip into extinction unnoticed" [40]. The better definition of conservation units or ECUs is a greater priority today than fixing the number of species, considering that taxonomy is particularly relevant when translocations are considered a key conservation component [105]. ...
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Ecotourism can fuel an important source of financial income for African countries and can therefore help biodiversity policies in the continent. Translocations can be a powerful tool to spread economic benefits among countries and communities; yet, to be positive for biodiversity conservation, they require a basic knowledge of conservation units through appropriate taxonomic research. This is not always the case, as taxonomy was considered an outdated discipline for almost a century, and some plurality in taxonomic approaches is incorrectly considered as a disadvantage for conservation work. As an example, diversity of the genus Giraffa and its recent taxonomic history illustrate the importance of such knowledge for a sound conservation policy that includes translocations. We argue that a fine-grained conservation perspective that prioritizes all remaining populations along the Nile Basin is needed. Translocations are important tools for giraffe diversity conservation, but more discussion is needed, especially for moving new giraffes to regions where the autochthonous taxa/populations are no longer existent. As the current discussion about the giraffe taxonomy is too focused on the number of giraffe species, we argue that the plurality of taxonomic and conservation approaches might be beneficial, i.e., for defining the number of units requiring separate management using a (majority) consensus across different concepts (e.g., MU-management unit, ESU-evolutionary significant unit, and ECU-elemental conservation unit). The taxonomically sensitive translocation policy/strategy would be important for the preservation of current diversity, while also supporting the ecological restoration of some regions within rewilding. A summary table of the main translocation operations of African mammals that have underlying problems is included. Therefore, we call for increased attention toward the tax-onomy of African mammals not only as the basis for sound conservation but also as a further opportunity to enlarge the geographic scope of ecotourism in Africa.
... Among mammals, and following from studies by Groves (2001) and Groves and Grubb (2011), the dPSC has been applied to primates and ungulates (Wilson and Mittermeier 2011;Mittermeier et al. 2013) with varying levels of acceptance. While this approach has been readily followed for primates, there is a strong lack of consensus among those who work on different ungulate taxa (Heller et al. 2013;Gippoliti et al. 2018). For example, while Burgin et al. (2020) primarily use the PSC for all mammals, they then cite notable exceptions among ungulates. ...
... Resources could be wasted if too many taxa are recognised beyond what would seem justified ("taxonomic inflation"; e.g., Isaac et al. 2004;Zachos et al. 2013Zachos et al. , 2020Simkins et al. 2020) and species conservation could be compromised by inbreeding in small population fragments that should be recognised as conspecific. Alternatively, we may not be recognising sufficient species diversity ("taxonomic inertia"; e.g., Gippoliti et al. 2018) and hence risk losing species inadvertently through ignorance, if data are limited. Following traditional classifications that have little or no scientific merit, resulting potentially in an either overor underestimate of species diversity, can thus impede anticipated conservation outcomes. ...
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... Widely distributed species has often neglected in conservation planning considering their large population sizes, occurrence into varying habitats and their inherent adaptive potential to respond changing climatic conditions (Chevin et al. 2010;Gippoliti et al. 2018;Thakur et al. 2018). Under the widespread species, classifying various populations into management units (MUs) or evolutionary significant units (ESUs) is vital for prioritizing genetically distinct populations which often deserve to be managed differently at regional scale (Moritz 1994;Ryder 1986;Singh et al. 2015). ...
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... Taxonomy, which requires rigor in the delimitation between taxa, involves, in a modern integrative approach, a painstaking and time-consuming labor encompassing morphological, ecological, ethological and genetic studies on a large number of specimens and populations (Padial et al. 2010). On the other hand, conservation may require rapid taxonomic decisions to help legislators, policy makers and stakeholders to introduce a priori conservation measures in the effort to protect populations of alleged biological importance from extinction or from the obliteration of their habitats before it is too late (Gippoliti and Groves 2013;Gippoliti et al. 2018). However, rapid taxonomic decisions may lead to "taxonomic inflation" (Alroy 2003;Isaac et al. 2004) and, what is worst, may result in the proliferation of poorly supported taxa (Zachos et al. 2013). ...
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... However, this needs to be studied further with genome-level data and more samples collected from both sides of the river. The study declared that understanding of distribution boundary between two species will halt the inappropriate conservation action and will avoid detrimental interbreeding between the two species in captivity [54,55]. This kind of future study will help to gain insights into the effects of geological events on the population divergence and distribution of allele frequencies in the landscape which provide vital information for making species recovery programs [56,57]. ...
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... It has been understood for many years that inadequate or ambiguous taxonomy and nomenclature for species can have negative impacts on conservation, medicine, and other fields ("taxonomy as destiny", May, 1990; see also Daugherty et al., 1990;Thomson, 1997;Frankham et al., 2012;Sangster & Luksenburg, 2014;Gippoliti et al., 2018;Christenhusz, 2020;Lücking, 2020;Freemann & Pennell, 2021). This happens in part because taxonomic names are often used as though they are stable hypotheses, when in fact taxonomies often have a degree of uncertainty and flux. ...
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... Often, lack of objectivity in taxonomy has produced a splitting frenzy trend, which is potentially threatening species conservation (Zachos 2013;Mori et al. 2019a;Zachos et al. 2019). Conversely, lumpers, i.e. those authors less prone to splitting, are accused of taxonomic inertia which may in turn prevent important management and conservation actions (Groves et al. 2017;Gippoliti et al. 2018). ...
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... For the many mammals threatened with extinction (Tilman et al., 2017), including carnivores and ungulates, changes of the underlying taxonomy can have direct consequences in terms of conservation efforts (Brownlow, 1996;Gippoliti et al., 2018;Thomson et al., 2018), with species often more valued from a conservation standpoint than are subspecies or local populations (Isaac et al., 2004;Mace, 2004). Examples where taxonomic uncertainty has the ability to threaten conservation efforts can be found in several threatened North American small carnivores including the pygmy raccoon Procyon pygmaeus and dwarf coati Nasua nelsoni (McFadden et al., 2008), island fox Urocyon littoralis (Hofman et al., 2015), and San Joaquin kit fox Vulpes macrotis mutica (Dragoo and Wayne, 2003). ...
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Invited contribution to the Symposium Volume celebrating the 225th anniversary of the Zoological Museum of Lomonosov Moscow State University The Tentelic Thesis explicates the attributes and roles of collections of preserved natural science specimens in epistemology. Combining the Latin roots (Tena — to hold, with Tela — a web), tentelism describes how specimens inform the sciences; specimen preservation maintains the fecundity, fidelity and veracity of both existing and future knowledge. Natural science collections preserve tentelic specimens as the focal sources of scientific verification and innovation. The tentelic attributes of specimens hold two interfacing roles in the changing landscape of science. They maintain the veracity of existing knowledge; and they equally catalyse new discoveries across the frontiers of scientific exploration. Alongside verifying and refining published knowledge, tentelic specimens are centrally positioned to support and inform a spectrum of unanticipated discoveries. The maturation of 21st century science expands and elevates the core roles of collections in generating knowledge. Burgeoning refinements in analytical methods enable new insights from old specimens. Advances in methods developed in the Earth and life sciences are exemplified in how analytical instrumentation quantifies minerals, biochemicals and organismal structure at the molecular scale. These advances hinge on refinements of the Principles of Specificity, which increase the resolution and precision of scientific methodologies. Continuing advances in genomics and geochemistry open up new opportunities to explore collections, and in driving the emerging integration of the earth and life sciences, increase the relevance and scope of the Tentelic Thesis. I argue these developments are focused in the emergence of geobiology, which consolidates Earth System science. Geobiology creates unprecedented opportunities to integrate tentelic information in biodiversity collections into a geological framework. This is because the chain of epistemic dependency extends from collections through natural history to support earth system science. Collecting and preserving are still the core operations in natural history, ever since these roles became established in the 19th century. To avoid repeating past mistakes, we need to understand the significance of this emerging consolidation of natural history, because the triumphant voyage of the sciences through the 20th century carried natural history as a barely tolerated stowaway. Continuing progress in analytical applications by improving access to collections, is set to expand applications of tenetic evidence across Earth systems. The emergence of geobiology teaches us how the armamentarium of molecular tools opens up unforeseen opportunities: empowering reexaminations of old specimens that allow us to ask entirely new questions. The history of science reminds us that we can only guess at future methods and questions. The challenges of Earth Stewardship in the Anthropocene underscore the importance of this quest, especially where it bears on the ecological integrity of Earth’s Critical Zone and biodiversity conservation.
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