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What constitutes a ‘native’ species? Insights

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Article in Biological Conservation · June 2015

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 Biological Conservation 186 (2015) 143–148

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Perspective

What constitutes a ‘native’ species? Insights from the Quaternary faunal

record
Jennifer J. Crees ⇑, Samuel T. Turvey
Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK

a r t i c l e i n f o a b s t r a c t

Article history: The ability to make decisions regarding a species’ native status according to appropriate environmental
Received 9 December 2014 baselines is of vital importance for current-day environmental management, particularly as non-native,
Received in revised form 26 February 2015 invasive species eradication has emerged as a key focus of conservation and ecology. Most definitions of
Accepted 6 March 2015
native preclude any human influence, yet the longer-term faunal record reveals a more complex picture
of changing species distributions in response to both environmental change and human activity, which
have altered regional biogeographic patterns for tens of millennia across the Late Quaternary. We there-
Keywords:
fore propose a new framework that outlines possible sub-categories that exist between the current ‘na-
Baselines
Biogeography
tive’/‘non-native’ dichotomy, incorporating information and examples from a range of Quaternary
Colonisation sources (palaeontology, zooarchaeology, historical archives, and ancient DNA). This framework is
Human impacts intended to encourage more nuanced debate and perspectives around human–faunal interactions past
Non-native and present, and to inform management decisions within ecology and conservation.
Reintroduction Ó 2015 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
1.1. The influence of past Quaternary environmental change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144
1.2. Length of time a species has been regionally present. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
1.3. The extent to which humans have facilitated a species’ presence and establishment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
1.4. The genetic identity of native species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
2. Implications for defining native species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
3. Applying the framework to management and policy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
4. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147

1. Introduction restricted (typically decadal-length) time-scales employed in ecol-

There is considerable need to agree upon a common under-
standing of what a native species constitutes, for both ecological
research and management purposes. Surprisingly, whilst there
has been much interest in defining a general framework for under-
standing the impact of invasive species (Blackburn et al., 2011), the
concept of ‘native’, as the starting point for biological invasions, has
rarely been explicitly considered. This is partly due to the
⇑ Corresponding author. Tel.: +44 (0)20 7449 6322.
E-mail address: jennifer.crees@ioz.ac.uk (J.J. Crees).
ogy (Willis and Birks, 2006), which fail to account for past climati-
cally-driven environmental change or historical and prehistoric
human impacts that have substantially influenced the composition
and function of ecosystems across much of the world throughout
the Late Quaternary onwards. Decisions regarding the classifica-
tion of native versus non-native species are also based on more
than ecological rationale alone, as species can have cultural or his-
torical significance that may influence judgements on their native
status. Our ability to define these categories as objectively as pos-
sible, using multiple lines of evidence, is therefore particularly
important.

http://dx.doi.org/10.1016/j.biocon.2015.03.007
0006-3207/Ó 2015 Elsevier Ltd. All rights reserved.
144 J.J. Crees, S.T. Turvey / Biological Conservation 186 (2015) 143–148
Commonly accepted definitions of ‘native’ include those of the
International Union for Conservation of Nature (IUCN) and the
Convention on Biological Diversity (CBD), which define a native
species simply as one that occurs ‘within its natural range’ (IUCN,
2014a; Convention on Biological Diversity, 2014). Others have
explicitly included a temporal component to clarify the possible
influence of humans, but these lack a consistently agreed timeline.
For example, Webb (1985, p. 232) considered that a native plant is
one ‘which evolved in [Britain or Ireland] or which arrived there by
one means or another before the beginning of the neolithic period,
or which arrived there since that date by a method entirely indepen-
dent of human activity’. This means that even pre-Neolithic intro-
ductions should be considered native, justified on the somewhat
arbitrary basis that the influence of pre-Neolithic humans on spe-
cies dispersal was ‘equivalent to that of animals’ as they were ‘part of
Nature’ (Pyšek, 1995, p. 72). On the other hand, Scottish Natural
Heritage (2014) suggested that native species are those which
‘migrated (or were transported by other species) into Great Britain
after the last Ice Age, without the assistance of humans’, and the
British Ornithologists’ Union Records Committee (2007) also sug-
gested a baseline of 16,000 years before present (BP) following
the Last Glacial Maximum (LGM). It is also unclear at which point
in time an established species that has arrived naturally may be
called ‘native’ or simply ‘naturalised’, the latter of which tends to
be attributed to species that have arrived more recently.
Appropriate longer-term environmental baselines therefore
need to be used to make informed judgements on what constitutes
a native species, and to identify those factors responsible for
changes in the distribution and persistence of different taxa. In par-
ticular, we require a more detailed understanding of the prehis-
toric and historical role of humans in this process, as the degree
of anthropogenic influence on the past movement of wildlife is
key to distinguishing between native and non-native species.
Botanists have previously developed terminologies that incorpo-
rate the influence of past human activity on plant biogeography
(Webb, 1985; Quezel et al., 1990; Usher, 2000), but these have
not been consistently adopted by the botanical or wider ecological
community (Pyšek, 1995). This may partly be due to the fact that
several of these frameworks pertain to specific geographic regions
and that many botanical classifications relate to unique modes of
plant movement, e.g. dispersal via fire, cultivation and grazing, that
are not consistently relevant for fauna as well as flora.
To help reframe the important debate over appropriate goals in
regional environmental management and restoration (Durant,
2014), we identify and discuss four major factors that need to be
taken into consideration when classifying native and non-native
faunas, and highlight these factors using relevant examples from
the Quaternary record. Within these discussions we also suggest
novel classifications for species status along a proposed ‘native to
non-native continuum’ to help refine and reassess the current
native/non-native dichotomy, which we summarise in Table 1.
We also illustrate how these classifications relate to different time
periods and the length of time since colonisations have occurred in
Fig. 1. Finally, we discuss the implications of this more nuanced
framework for environmental management and conservation.
1.1. The influence of past Quaternary environmental change
The global climate has fluctuated substantially across the Late
Quaternary, but the temporal baseline for defining a native species
has generally been the point when the Earth emerged from the
most recent glacial period, usually taken as either the beginning
of the Holocene Epoch around 11,700 BP, or after the LGM in the
terminal Pleistocene Epoch (British Ornithologists’ Union Records
Committee, 2007). Rapidly increasing temperatures and rising
sea levels associated with this climatic transition (Anderson
Table 1
Proposed framework for definitions of species states. Recent historical era defined as
post-AD 1500 following IUCN (2014b). These definitions do not all represent mutually
exclusive categories.
Species state Definition
Native Continuous presence since the Late Pleistocene, or
naturally (re)colonised during the Holocene
Synanthrope/commensal Native but has adapted to living in close
proximity to humans, usually due to some feeding
benefit, e.g. red fox, badger in Britain
Archaeofauna Introduced before recent historical era with no
previously known native status in a region, e.g.
rabbit in Britain; dingo; island fox; cuscus in SE
Asia
Restored native Previously native but regionally extirpated due to
human agency or natural environmental
processes; failed to recolonise naturally, but since
recolonised due to human intervention, e.g. fallow
deer, hare in Britain
Returned native Previously native but regionally extirpated due to
human agency or natural environmental
processes; recolonised without direct human
intervention, e.g. fulmar in Britain
Xenonative Native into recent historical era but reintroduced/
restocked population of wholly or partially
different genetic origin from original native
population, including possible domestic status,
e.g. wild boar, red kite, wildcat in Britain
Anthropofauna Dependent on human-modified environments;
geographic distribution mediated by human
migration or movement, e.g. house sparrow,
house mouse
Recent native Spread without direct human mediation during
the recent historical era, e.g. collared dove in
Europe
Neofauna (non-native) Introduced by human agency during recent
historical era
et al., 2013) drove a global geographical reorganisation of biomes,
with environments across northern Eurasia shifting from open to
closed landscapes (Allen et al., 2010). Species that disappeared dur-
ing or before these environmental shifts are rarely considered to
represent species that are in some sense still ‘native’. For example,
fallow deer (Dama dama), which disappeared from Britain prior to
the Holocene (Currant and Jacobi, 2001) and were later introduced
by the Romans and then the Normans (Sykes, 2010; Montgomery
et al., 2014), are classified as a long-standing naturalised species
(Ward, 2005). Likewise, reindeer (Rangifer tarandus), which sur-
vived in Britain until the early Holocene due to a short lag in veg-
etational succession (Coard and Chamberlain, 1999; Sommer et al.,
2014), were reintroduced to the Cairngorms in the 1950s due to
their former regional occurrence, but as a free-ranging semi-
domestic animal they are not considered to represent a fully
native, wild species (Hetherington, 2013).
Although the Pleistocene–Holocene transition marks the most
recent significant ‘natural’ influence on regional biogeography,
the close association between rapid climatic warming and subse-
quent sea-level rise meant that the northward expansion of some
species was halted only by the timing of land-bridge flooding.
This has resulted in continental-shelf islands such as Britain con-
taining assemblages of species united only by their presumably
more rapid dispersal ability. For example, white-toothed shrews
(Crocidura leucodon, C. russula) failed to reach Britain before the
flooding of the English Channel c.8600 BP (Anderson et al., 2013),
but occur naturally today as far as the northern French coast
(Yalden, 1999). Likewise, as there was probably only a brief land-
bridge between Britain and Ireland following de-glaciation
(Devoy, 1985; Lambeck, 1995), mammals such as beaver (Castor
fiber), elk (Alces alces), aurochs (Bos primigenius) and roe deer
 J.J. Crees, S.T. Turvey / Biological Conservation 186 (2015) 143–148
Fig. 1. Proposed categories of species states highlighting temporal periods across which colonisations occurred. Black arrows denote natural colonisation; grey arrows denote
direct human-assisted colonisation (i.e. transportation); dashed grey arrows represent indirect human-assisted colonisation, e.g. through landscape
modification/management.
(Capreolus capreolus) failed to colonise Ireland from Britain before
sea levels rose (Yalden, 1999).
The fact that regional mammalian biogeography was heavily
shaped by the historically contingent lag effects of climatic and
environmental change into the first half of the Holocene raises
important considerations for what we might decide constitutes a
non-native species. For instance, although roe deer failed to colo-
nise Ireland in the early Holocene, they had reached mainland
Britain by this stage and could presumably have also reached
Ireland naturally if the temporal dynamics of sea-level rise and
land-bridge inundation had differed slightly. They were in fact
later introduced to Ireland around 1870, although the population
only persisted for about 50 years before being extirpated through
overhunting (Prior, 1995). If this population had survived, it is
questionable whether we would consider it to have the equivalent
non-native status as that of the introduced roe deer population in
Pohnpei, a remote Pacific island which the species could never
have reached without human assistance, or that of the British pop-
ulation of Chinese water deer (Hydropotes inermis), which was
introduced from China in the late 19th century. This clearly has
implications for how we choose to manage certain non-native spe-
cies relevant to their geographical context.
1.2. Length of time a species has been regionally present
The Pleistocene–Holocene climatic transition also coincided
with final human colonisation of all the world’s continents other
than Antarctica (Goebel et al., 2008). However, human migrations
out of Africa and around the globe have been taking place for many
millennia, and there is increasing evidence for human transporta-
tion (‘ethnophoresy’) of non-domesticated species, either deliber-
ately (in the case of economically or culturally favoured
‘ethnotramp’ species, e.g. deer, pigs) or accidentally (in the case
of smaller-bodied ‘stowaway’ species, e.g. murid rodents), for at
least several thousand years (Heinsohn, 2002). The introduction
of dingo (Canis lupus dingo) to Australia c.5000 years ago
(Savolainen et al., 2004) is perhaps the best-known example of
such ancient human-mediated transportation, but others include
the probable introduction of island fox (Urocyon littoralis) to the
California Channel Islands c.6500 years ago (Rick et al., 2009), the
widespread introduction of Pacific rat (Rattus exulans) across the
insular Pacific region with the migration of Austronesian colonists
from c.3000 BP onwards (Matisoo-Smith and Robins, 2004), and
the introduction of rabbit (Oryctolagus cuniculus) to Britain by the
Normans in the 11th century (Yalden, 1999).
Such ancient animal introductions might be referred to as ‘ar-
chaeofauna’ (Table 1 and Fig. 1), by analogy with ‘archaeophytes’,
145
a term used in botany to refer to alien plant species that were
introduced and became established between the Neolithic and AD
1500 (in contrast to ‘neophytes’, which were introduced after AD
1500), and which are accepted by many botanists as now constitut-
ing native species (Preston et al., 2004). Indeed, some human-
mediated animal introductions are even more ancient, particularly
in Australasia. The earliest known translocation in this region is
the northern common cuscus (Phalanger orientalis) to New Ireland
between 20,000 and 23,500 BP; others include the common echymi-
pera bandicoot (Echymipera kalubu) and Admiralty cuscus
(Spilocuscus kraemeri), which were introduced to Manus by
c.13,000 BP, and the brown dorcopsis wallaby (Dorcopsis muelleri),
which was introduced to Gebe between 8500 and 10,000 BP
(Spriggs, 2007; Heinsohn, 2010).
Such ancient introductions necessitate a debate around
whether these species should be awarded the same status as truly
‘native’ species. Dingoes are now considered an important apex
predator in the absence of other extant Australian mammalian car-
nivores. Indeed, a recent study has argued that ‘‘the logical criterion
for determining native status of a long-term alien species must be once
its native enemies are no longer naïve’’, and used the example of
bandicoot predator avoidance as proof of the dingo’s native status
in Australia (Carthey and Banks, 2012). Similarly, the island fox is a
protected species on the California Channel Islands, and has even
been subject to a recent intensive recovery programme following
population decline (Coonan et al., 2010); and although the Pacific
rat is responsible for huge numbers of prehistoric extinctions of
endemic bird species across the tropical Pacific (Steadman, 2006),
in New Zealand it is regarded as historically and culturally signifi-
cant by many Maori.
In contrast, some species have colonised regions much more
recently – often within the recent historical era, so that detailed
ecological records are available on the dynamics of their range
expansion – but without direct human mediation, such that these
events may be termed ‘natural’. Some former British ‘returned
native’ bird species, such as fulmar (Fulmarus glacialis) and com-
mon crane (Grus grus) (Yalden and Albarella, 2009) and possibly
also little egret (Egretta garzetta) (Shrubb, 2013), have recolonised
Britain following a decrease in hunting pressure, to replace pre-
vious native populations eradicated through overexploitation dur-
ing past centuries (Table 1 and Fig. 1). Other range expansions
represent colonisations of new regions rather than recolonisations,
and such species might be thought of as ‘recent natives’ (Table 1
and Fig. 1). Probably the best-known example is the collared dove
(Streptopelia decaocto), a south Asian species that spread rapidly
across Europe from the 1930s and reached Britain in 1952, where
it is now abundant. Other examples include the 20th century
146 J.J. Crees, S.T. Turvey / Biological Conservation 186 (2015) 143–148
spread of cattle egrets (Bubulcus ibis) across Africa, Europe and the
Americas (Botkin, 2001), and late Holocene colonisation of New
Zealand by the Australasian harrier (Circus approximans) and pur-
ple swamphen (Porphyrio porphyrio), where migrant birds from
Australia appear to have filled avian niches left vacant by the
extinction of Eyles’ harrier (C. eylesi) and two species of takahe
(P. hochstetteri, P. mantelli) (Worthy and Holdaway, 2002). Are
these species to be regarded – and tolerated – as ‘natives’, if they
are colonising new regions without direct human assistance?
This is a pertinent and pressing management issue for ecologists
and conservation biologists; with the onset of climate change,
increasing numbers of species are likely to shift their ranges and
colonise new regions within their climatic/environmental niche,
as may already be occurring with the northward spread of species
such as Cetti’s warbler (Cettia cetti) into Britain (Stewart, 2004;
Chen et al., 2011).
1.3. The extent to which humans have facilitated a species’ presence
and establishment
As many of the examples above demonstrate, the nature of
anthropogenic influence on species introductions is not always as
straightforward as the deliberate physical transportation of ani-
mals from one region to another. Indeed, the collared dove inva-
sion was probably facilitated by increasing urbanisation and
habitat modification (Fujisaki et al., 2010), the spread of cattle
egrets was mediated by their ability to exploit pastures with high
cattle densities (Botkin, 2001), and the sudden availability of New
Zealand bird niches was the result of human-caused extinctions in
the endemic avifauna. The archaeological record also highlights
many other indirect ways in which humans have influenced
biogeography.
Humans first began directly altering landscapes around 45,000
BP in Australia through modification of regional fire regimes
(Rule et al., 2012), and the subsequent global-scale losses of
megafaunal mammals – arguably directly or indirectly mediated
by human activities – may have driven further shifts in plant com-
munities (Zimov, 2005). Substantial anthropogenic alteration of
landscapes through deforestation and agricultural expansion
began from at least 11,500 BP in the Near East (Zeder, 2011). As
increasingly open, farmed landscapes spread across Eurasia during
the Holocene, species that were pre-adapted to similar environ-
ments often followed. Some species, such as the house sparrow
(Passer domesticus), probably expanded their ranges without direct
human facilitation (Ericson et al., 1997), whilst for many other spe-
cies this process was less clear; for example, the house mouse (Mus
musculus) had spread to Europe from Asia by the Iron Age (c.1000
BC), but could have been either deliberately introduced to Britain
or arrived accidentally on sea-faring vessels, possibly from two dif-
ferent routes (Searle et al., 2009). However, the pre-requisite for
survival and establishment for these species was the continued
presence of human-managed, open landscapes and settlements.
They might therefore be termed ‘anthropofauna’ (Table 1 and
Fig. 1).
Several species that are now widely regarded as native to
Britain actually disappear from the regional palaeontological and
archaeological record after open landscapes were replaced with
forest at the end of the Pleistocene, and then reappear in the
Mid-Late Holocene, presumably as the result of subsequent rein-
troduction. These species might therefore be thought of as ‘re-
stored natives’ (Table 1 and Fig. 1). For example, brown hare
(Lepus europaeus) and harvest mouse (Micromys minutus) were pre-
sent in the Late Pleistocene of Britain but are both absent from
Mesolithic and Neolithic sites, with possible evidence for their
reappearance in the Bronze Age and confirmed evidence by the
Iron Age (Yalden, 1999). However, as their temporary
disappearance is based on an absence of evidence, and as small
mammal remains are rare in the Mesolithic, their non-native status
may still be questioned. More convincingly, there is lack of evi-
dence for great bustard (Otis tarda) in Britain from the end of the
Pleistocene until the Medieval period, when it was probably rein-
troduced for hunting (Yalden and Albarella, 2009; Shrubb, 2011).
Successful re-establishment of these species was almost certainly
facilitated by deforestation and the spread of more open, agricul-
tural landscapes in Britain.
Even among uncontroversially native taxa, certain species
appear to benefit from human presence more than others; these
species are often called ‘synanthropes’ if they have adapted to live
alongside humans, or ‘commensal’ if this also confers some feeding
benefit (O’Connor, 2013) (Table 1 and Fig. 1). For example, red fox
(Vulpes vulpes) can readily exploit resources in urban spaces, and
badger (Meles meles) also benefit from the concentration of inver-
tebrates and small vertebrates in urban gardens, with urban bad-
gers in Britain showing reduced home range size and increased
population density (O’Connor, 2013). Similar adaptations are also
seen in stone marten (Martes foina) populations in mainland
Europe (O’Connor, 2013). More directly, the survival of native red
deer (Cervus elaphus) populations in Britain has been ensured
through establishment of deer parks and management for hunting
and recreation (Ward, 2005). The increased ability of all of these
species to tolerate and exploit anthropogenic environments has
certainly contributed to their continued success across their native
ranges.
1.4. The genetic identity of native species
Several extirpated native species have subsequently become re-
established through deliberate or accidental releases, but these
replacement populations are often genetically distinct from pre-
viously native populations, and thus might be termed ‘xenonatives’
(Table 1 and Fig. 1). For example, wild boar (Sus scrofa) has re-
established in several parts of Britain through escapes from farms,
but many of these populations contain domestic pig hybrids
(Wilson, 2005). Other British species, such as roe deer, crane and
red kite (Milvus milvus), consist of remnant native or natural reco-
lonist populations that have been supplemented with individuals
from mainland Europe to increase their viability (Evans et al.,
1999; Yalden, 1999; Sainsbury and Vaughan-Higgins, 2012). The
genetic status of other native species is being altered through
hybridisation with domestic or feral counterparts, for example
Eurasian wildcat with domestic cat (Felis catus) (Oliveira et al.,
2008; O’Brien et al., 2009). These examples not only raise further
questions over what constitutes a ‘native’ population, but also over
the potentially variable goals of assisted colonisations and reintro-
ductions for conservation. Such programmes may aim either to
restore former regional species composition, or former ecosystem
processes such as rooting of forest vegetation by boars. Indeed,
the latter is often cited as the goal of many so-called ‘rewilding’
projects concerned with the effects of past human-caused removal
of former keystone species (Zimov, 2005; Donlan et al., 2006;
Griffiths et al., 2011), but which may be achieved using extant eco-
logical substitutes rather than now-extinct native species.
2. Implications for defining native species
The issue of defining a native species is of more than semantic
interest, as the ability to make informed decisions on management
or eradication of invasive species and restoration of native species
is a vital part of modern ecology and conservation. For example,
justification for the recent, high-profile reintroduction of great bus-
tard to southern England comes from historical evidence for extir-
pation of an apparently native British population during the 19th
 J.J. Crees, S.T. Turvey / Biological Conservation 186 (2015) 143–148
century (Osborne, 2005). However, the longer-term Quaternary
record challenges the bustard’s native status, and whilst Britain
now contains artificially open landscapes suitable for bustard, cur-
rent conservation management for the species is arguably based on
incomplete scientific evidence of its native status due to the use of
relatively recent (century-scale) ‘historical’ baselines.
As we hope to have demonstrated, defining what constitutes a
native species is not necessarily as straightforward as is usually
assumed and there are indeed ‘shades of nativeness’ (Usher,
2000). In order to understand the status of different components
of regional biodiversity that can in turn inform conservation or
ecological restoration, we need to extend the timescales that have
typically been employed to define native faunas, even beyond the
historical record, as demonstrated by the great bustard example.
Indeed, we are still discovering what constitutes the native
British vertebrate fauna, despite well over a century of study.
Ancient DNA analysis has recently determined that a gadfly petrel
(Pterodroma) population recorded from Scotland during the
Holocene, which probably survived until black rats (Rattus rattus)
were introduced during the Roman period, was phylogenetically
distinct from all other extant Pterodroma taxa (Brace et al., 2014).
Molecular techniques have also revealed the probable natural colo-
nisation of Ireland by pike (Esox lucius) 3500–4000 BP, in addition
to a more recent anthropogenic introduction around 1000 BP
(Pedreschi et al., 2014). The pool frog (Pelophylax lessonae) was for-
merly misclassified as non-native, but zooarchaeological and archi-
val records, genetics and bioacoustics eventually confirmed its
native status, ironically just as the last British population became
extinct (Beebee et al., 2005; Snell et al., 2005). Similar revisions
of native status are also being made in many other regional faunas.
For example, ancient DNA analysis of Holocene fossil dung from
Tiburón Island, California, has recently demonstrated that bighorn
sheep (Ovis canadensis) were native to the island; their introduc-
tion in 1975 thus constituted an example of ‘unintentional rewild-
ing’ (Wilder et al., 2014).
It is therefore vital that multiple lines of evidence, including the
historical, zooarchaeological and longer-term Quaternary records
as well as modern molecular techniques and other sources of data,
are all used to inform ecological debates around native and non-
native species (Lyman, 2006; Dietle and Flessa, 2011). We also
need to revise our sometimes simplistic understanding of past
human influences over biogeography. Human activities have had
profound and long-lasting impacts on the dynamics and success
of both natural colonisations and anthropogenic introductions of
species to new regions for many millennia, through alteration of
landscapes and distribution of resources as well as physical move-
ment of organisms. An improved understanding of these processes
across space and time will permit more nuanced debate over
native species conservation and management.
3. Applying the framework to management and policy
The complexity of the natural world, and the ways in which we
have influenced it, generally defies our human instinct for simplis-
tic classification and compartmentalisation. Furthermore, the
broad terms ‘native’ and ‘non-native’ typically entail some kind
of value judgement, particularly reflected in how we choose to
manage different species, and therefore it is vital to begin with a
more detailed understanding of what such terms encompass.
This paper is not an exhaustive exercise, but an initial framework
for re-thinking what it means for a species to be considered ‘na-
tive’. We hope that this will stimulate debate that could potentially
contribute towards further development of such a framework.
Decisions related to the removal of non-native, invasive species
are currently made on a case-by-case basis, and we would endorse
147
this process. We are not proposing or advocating the blanket redef-
inition of species within this framework to justify their restoration
or eradication. We present this as a framework that could help
guide management decisions on an individual species basis rela-
tive to the region of interest and the management aim. Most global
landscapes have been subject to partial or complete modification
by humans, and this is now the context in which we must carry
out protection of species and ecosystems from further degradation.
Some anthropogenic landscapes have even served to enhance
biodiversity and provide novel conservation opportunities.
Moreover, ecosystems are dynamic entities and require being
thought of as complex, changing systems within which species
have evolved and adapted, thus precluding simplistic management
responses.
Above all, we need to be able to have well-informed debates in
science and policy around species that a particular country or
region wishes to classify as native or non-native (and potentially
by implication as invasive). For example, this issue formed part
of legislation recently debated in the UK Parliament but that lacked
any scientific basis, potentially posing a risk to biodiversity
(Durant, 2014). Furthermore, breeding and reintroduction of spe-
cies are costly undertakings, and in a world of finite conservation
resources we need accurate information on the status of species
in which we may want to invest.
4. Conclusions
Whilst there has been exponential growth of interest in inva-
sion biology and the ecological impacts of non-native species in
recent years, the question of how we define a native species has
been surprisingly underexplored. We use evidence from the long-
term Quaternary faunal record to highlight examples of the
dynamic turnover in regional species composition over many mil-
lennia due to both natural and anthropogenic factors. However,
this consequently opens up a far wider debate regarding where,
and how, we draw baselines to decide what constitutes ‘natural’
and ‘native’. We have therefore proposed a new lexicon to explore
the space between ‘native’ and ‘non-native’ that we hope will
stimulate debate in this area in order to inform both ecological
research and applied conservation management, in particular spe-
cies reintroductions and rewilding.
Acknowledgement
We thank Tim Blackburn for comments on an earlier draft.
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