Title Mammalian tolerance to humans is predicted by body mass: evidence from long-term archives.

Authors Crees, JJ; Turvey, ST; Freeman, R; Carbone, C

Date Submitted 2019-06-24 This article isprotected rights by All copyright. reserved. 10.1002/ecy.doi: lead todifferences version between this andthe ofPleasec Version Record. been and throughtypesetting, proofreadingwhich may thecopyediting, process, pagination This article undergone has for and buthas accepted been not review publication fullpeer 2 1 CarboneChris Robin Freeman Samuel T. Turvey Jennifer Crees J. Running Head: archive Title: typeArticle : Articles Department AcceptedInstitute Zoology,of Zoological Society London, of Regent’s Park, London,NW1 4RY, UK Article Mamm s

of Earth Sciences, Natural History Museum, Cromwell Road, London, SW75BD, UK a 1

1 lian t

1 Body mass predicts mammalian decline ,2 1 *

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olerance humans to

is predicted by body mass: evidence from long

ite th is article as - term

This article isprotected rights by All copyright. reserved. considered be to responsible, at least part,in for global Humans likely are have to driven biodiversity loss for Introduction population density Keywords: mammals, extinction emphasiz insights into human impacts. HPD HPDslower strongly body with mass, with larger specific tolerance a stability terrestrial novel due to restricted temporal and spatial scales present Humans Abstract * gainst E

Accepted Article mail:

for for continent “ . a high extinction filter However, o [email protected] that captures major transitions humanin demogr are different

ing mammal

implicated as the the than smaller the role the of long -

resolution database of human population -

wide T dynamics of s

his ecological pattern species

s to changing HPD through th

ur across across data

predictive understanding of s ” -

, set b resulting from understanding apoor

a major and therefore has wide odied mammals.odied the the

-

term understanding in archives containing prehistoric Holocene

filter

driver of species extinctions - at which bodied mammalsbodied experiencing regional population losses at , extinction risk, historical ecology, is

country extinction (c.11,500 years

confirmed across

O

ur this e Holocene -

analysis level

applicability for determining process s human

and

millennia last -

density (HPD) estimates to

and population the modernthe biodiversity crisis

ap to present), enables - -

caused extinctioncaused occurrence occurrence . i

hy s wide spatiotemporal Mamm human typically .

of pastof We from , with anthropogenic activities widely

us to a analyz -

lian caused biodiversitycaused loss the Latethe Pleistocene to the an species declines records assessed - identify levels of tolerance to level extinctions e

thresholds poch e Holocene, human

regional extirpationsregional remains poor

for of relative climatic , biotic

and the

scales 30

identify to HPDto European vulnerability to . ,

,

We We develop

and risk provid from due to scale s species .

of

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bias the

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This article isprotected rights by All copyright. reserved. population Acceptedextinctions only aurochs ( spatiotemporal scales rather than studying and past present extinctions in isolation. level point of a patterns of species responses human to pressures already become extinct typically based only onrecentecological persistence or extirpation presence aof species might bein habitat loss are both linked human with vulnerable offtaketo fromhunting individuals into increased Articletypically than smaller overharvesting is increase typically species typically current human presence assuch hunting and habitat loss and theof Pleistocene Svenning There There is already abody of ecological evidence associating The sustainability of species’ harvesting rates

European event

extinctions, Bos primigenius require potentially long - , level losses

(Temple and Terry 2007) and therefore it vital is understandto current - bodies species

20 large

is is 1 bigger have lower rates of reproduction than smaller species

more 5 decline and across therefore ) and predict . mamm Mammals particular in are highly susceptible extinctionto from human activit

likely drive to local extirpation globalor extinction of larger in due past to home ranges,

)

( - with with increasing body mass several other contact with people in fragmented habitats , which became globally extinct in Woodroffe 2000 term

al (Brook & Bowman 2005; Zuo 2013) al. et crucial

the Holocenethe

extinction ing process ( fluenced by Ripple et al. 2014; 2015)

future biotic vulnerability ( anthropogenic

Ripple et al. 2014; 2015 for for . However, making themmore sensitive habitat to loss

European mammal reconstructing population of of cumulative population losses

following systems from most which the susceptible species have ; up to the present

Karanth et al. both both this fails to acknowledge ( activity Faurby and its body

is IUCN’s cutoff of AD density

( linked

Woodward et al. 2005 the the - day mammalday extinctions over wide , .

dynamics and drivers of 2010 with with mass species (HPD), Understanding

) strongly (Ma . If levels of direct exploitation and to AD Svenning 2015)

HPD projected human population growth. ) an

. and cPhee 1999; Turvey 2009

1627, Ho , “

we might expect that such as elk ( extinction filter

wever, such HPD to with patternswith of where they bemore can . ,

Larger body mass and so rates population of

is is rather than asingle 1500 for assessing species . severe historical often mammalian

) . . - As a result,

bodied bodied species also E

documented Alces alces xtinction and analyses are . Larger historical For example, the ” - bodied speciesbodied

masking brin mammalian

tolerance to the ging - is theis end - ; bodied bodied

era era ), ), , species

Faurby

regional as as the and

true true

ies -

This article isprotected rights by All copyright. reserved. Accepted vulnerability to changing human pressure and HPD scale ecol understand mammalian extinction dynamics frommodern archives we remove regional time compared to population and species to losses be more easily present capturing agricul Articlehuman activity, from small GoldewijkKlein et al. 2010) deposits historical and archives f detailed Holocene record documenting human and highly variable both spatially andtemporally (Crees et al. 201 assessed hydruntinus continent European bison ( ogical

The quality long of In to investigate order the relationship between human presence andmammal persistence through we integrate across Europe, tural communities and recent . T

extirpation at at the - across space and time he broadly stable postglacial climate of the Holocene also allows wide level archives )

those ( Barnett

regional variation extinction 6 Bison bonasus d )

.

during datasets derived from zooarchaeological the and historical records reconstructto

with estimates of historical

chronologies the extinction the filter cumulativeof past population losses that biascan efforts to to et alet

investigate patterns of species presence or absence relationin body to mass landscape - term data in

the the of . 2006

- human pressure scale . Holocene Europe also encompasses several orders of magnitude of species such as more variable climat , and ) andmost of Europe’s large carnivores (Crees rom 11,500 around years ago to the present ; , low

for European mammals across the Holocene. Crees and Turvey 2014).

scale for reconstructing population past industrial generate - density ,

as as this is the spatial scale whichat population losses occur s .

s

lion . on

ized However, a new, hunter HPD attribut global ( Panthera leo

ic conditionsic and wild - available at predictive gatherer environments ed urbaniz mammal Europe has particularly a well

- to to day data E direct xtinction should

communitie ed societies )

understanding of of the and a similar landscape occurrence or

alone. , both historically and in the

European wild ass

distribution indirect Late

We combineWe s largerto settled (Roberts 1998) Pleistocene documented

(e in human activity therefore ideally . et al

g By using long zooarchaeological .

s

species Benecke 1999;

and dynamic . 2016 - level -

d resolved and (Turvey 2009) ( mammal

Equus - these ), ), specific specific , thus

spatial spatial or - term earlier be s

is

.

This article isprotected rights by All copyright. reserved. reported species due to the interpreted as a aspeciesof within a region, majority the of older historical many recenthistorical dates appearance of s historical literature (e.g. death of the last known aurochs Poland in in ( Where possible, historical data consistently theat country level native species native smaller occurrence data threshold species for which Europe only represented n=3 terrestrial mammal species developedWe a novel dataset of country Data collection Methods AcceptedData S1 Article 0

from different sou Resolution of last ;

Data S1 European mammal - (Signor and Lipps 1982) bodied , the most recently published directly dated record was : : Table

and ecological represented fact that the youngest fossil found will rarely ever if represent the true individuallast of a for , and translocated or reintroduced populations of : : Table

pecies thein zooarchaeological record associated with broader time intervals. Whilst species), but which also provided a sufficiently large dataset for robust analysis. terminus post quem all 30 consistently S data 1 ) ,

. as this

on the smallest body mass S species - rces. occurrence data ranged from specific calendar dates recorded in the recent 1

country ) literature . This populations werepopulations

with a with constituted Data on regional extirpations were gathered almost certainly represent (as the zooarchaeological(as and historical records are generally poorer for across millennial timescales

approach - . Where more than one zooarchaeological level

native Holocene range using most the recent published information for each species

preceding final extinction rather than anabsolute extirpation date,

extirpation the - level extirpations exclud finest the included for

margin their of

ed

spatial resolution that could be maintained which we were able to source regional last s

were range

(i.e.

the the true date

verified from - that that restricted exc

given quality the andquantity of regional from and zooarchaeological dates were luding introduced populations of occupied >5% global

Europea used 8000 BC AD to 2000

high of the . Vagrant individuals and range. AD >1 n - from

elevation

species independent data source

1627), to the knownlast death of the final individual last

A 2 of of - the the occurrence occurrence Europe’s area

kg bodymass ). ). zooarchaeological

D species ata wereata collected

for ,

date

all large and -

/or (> 2(> kg; non

was .

Only

- , This article isprotected rights by All copyright. reserved. become comparable mass in modern to cattle ancestor closely related extinct logged analysis for specific HPD ( absence Ga areas of HPD such as large urban cent remained relatively mobile and however country Goldewijk et al. 2010) combinations totaled 541 (Sommer al. et 2011) understood due to its potential misidentification with dome extirpation of wild horse ( uncertain, data for those countries w countries Italy,in Ukraine Austria and d 1980s, so these countries were excl Germany Czech andthe Republic but with breeding by AD 2000.For example transient

Acceptedl Article è s 2004) Information on Holocene Mammalian body mass data were -

level averages record , B. primigenius populations were excluded unless there was reasonable evidenc

were included our our study conducted is .

The The time bins provided by the HYDE data Data S1: Table s for each species in each country . Data for , so data for these countries were excluded.

E. hydruntinus

f and logged , rom (Arnold et al. 2012) which knownis to have

( Equus ferus Data S1: 2 Table 8 the Asiatic wild ass ( 000 BC AD to 2000 S o HPD

were maintained 2 appear to have across ). .

uded from the species’ extant range, whereas vagrant populations , M

was obtained from the HYDE ere golden jackal ( , and data for ean HPDean could be strongly influenced by high ) across) many er

taken from PanTHERIA the database(Jones et 2009)al.

millennial timescales s only arose in the last omitted from analysis. the For example, the timing of no ) . Where extinction .

(Wright and Viner firm evidence for established populations since the become

at at low densities. By contrast across experienced a size reduction thein Holocene . Gridded E

domestic Canis aureus quus central Europeancentral

base the Holocenethe established in the past few decades

hemionus stic horse stic in zooarchaeologicalthe record HPD

cattle were used to , when

- couple of date informationdate for aspec -

) ha) The Daniels 2015)

data

) global population (

Bos taurus

were used as a proxy for the most s final

that were associated with a countries been intermittently recorded in ( N e for establishment and/or centur /km human populations define number species of 2 , ) ) highly

. were extrapolatedwere to ies

were used for its wild is

a series presenceof

very poorly in Europein - database density areas concentrated ies wasies ,

so - (Le (Le country

( to to Klein Klein these

and ;

-

This article isprotected rights by All copyright. reserved. 99 2006). silvestris distribution corsac fox ( slopes are presented 95%± CI. by asimple linear regression through points the against calculated using ROC curves are presented in Figure calculated using ROC curves) the lowest false positi balance models towards the larger subset (either presence or absence) whereas the use ROC of curves aims to (ROC) curves determineto optimum thresholds for wedata, larger extinct species. imbalanced dataset containing relatively more presences for smaller extant species than absences for ferus database towards AD 2000 presence HPD initially calculated at whichat a species would be predicted becometo extinct and individual species Data analysis

Acceptedth Article

calculated centile ofcentile the HPD in the countries where they were In to investigate order species

by e.g. et Woodroffe (2000).al. However, a and CHPD was also

species sensitivity ) was also) excluded dueto poor quality presence of therefore also

data Felis silvestr s Vulpes corsac

in Europein and so had beto excluded from analyses

than absence data a body mass “ critical

country and specificity p ve rate T

is

calculated individual species CHPDs = 0.5 approximated o account for potential bias in the relative pr ) from) dataset final the ” ) , -

,

, well as as the removal some of earlymammal extirpations (e.g. level human population density

and the scaling relationship between CHPDs body and mass wasprovided had too few data points to calculate a .

following comparable studies Both sets of

are

Some

due increasedto frequency temporal of sampling the in HYDE presence provided for modelsfor by finding highest the true positive rate together with - specific specific

for species that experienced no extant -

absence dataabsence CHPD

in in thresholds of tolerance to HPD species, such as Data S

due to poorer data quality (

solid grey and line band, cross thresholds all 1: Table

2 (

CHPD) . species species our using logistic regression Individual CHPD

stil across its range

entire dataset there was higher a amount of investigating mammalian tolerance to

l - ( us absence data Asian badger ( present in AD 2000. those calculated S

threshold models. ing 3 .

for for reference The EuropeanThe wildcat CHPD

receiver operating characteristic oportion presence/absenceof localized A threshold p of = 0.5biases

)

for each species threshold dueto restricted .

. resultedThis a in slightly

threshold Figure 2 (Sommer and Benecke CHPD ,

Meles leucurus we first at , but only those

extirpations, using the

(present~ p

threshold = ). ). s were

0.5 analyzed All estimates of

, (

and those Felis ( log10( i.e. the HPD then s )

Equus and were

plotted hpd

) ) ,

This article isprotected rights by All copyright. reserved. AcceptedCriteria (AIC differentin models additional country were (present~ using logistic regression Cromsigt al. et 2012; Holocene habitat associations and the wider ranging range, modern and over past Holocene mammal populations (Collen et al. 2011) are 2014) Articlerespectively arctos database (Jones et 2009)al. included trophic mass over large such size ranges mammals of et (Jetz al analys history traits explicitly explored the effects of life history variables additionin HPDto those species which had very absence few points continent known to be associated with P We comparedWe . resence ) e Other species s have broad omnivorous diets behavior of on - log10( wide are potential

, due low to sample size for analysis (Bojarska & Selva 2012; the effects of variation in

(e.g.,

), and the model andthe ), with the lowest AICvalue wasinterpreted as having best the included as - also absence data for all species and countries were

analysis hpd level (herbivore /carnivore) as a further predictor variable the the - reproductive rate

four day ( )

conditions. For example, impact trophicof level species Data S + - specific ecologicalspecific variables Fyfe al.et 20 log10( subjects

home range models that : : (present~ random effect 1: 1: Table . T

historically mass allowed us to

wo of

investigating variation in ) continuing

species our in database ) vegetational composition of European landscapes during the 1 log10( ,

) estimates S 3 and (present~ , so

are likely to i ) 4 body mass . )

. s present

. these species Models , hpd

We alsoWe generated three further models exploring the

could not be included ourin analyses due uncertainty to incorporate , included both as an additional and as an interaction term extinction

debate

) h the the relationship between HPD and species from ), (present~), ome range with

, were ranked according to

( because log e.g. such home as range and habitat association, which nfluence tolerance HPD,to we

outside Europe and uncertainty in in 10 , were

both both Europe Eurasian vulnerability or resilience in modern ( .

hpd

2004 ( log varies greatlyvaries these traits are wild boar extinct and extant species assigned as ) 10 * then ; ; Woodward et al. 2005 . Both log10(

( mass otter otter also may not

(

Sus scrofa mammalian species mass e.g., ) Lutra lutra ), ),

combined into a single herbivore across a species’ geographic . strongly correlated with Mitchell 2005; ) Ballari & Barrios Although

), the the following PanTHERIA the be

where species Akaike Information represent ;

brown bear ) , and which also focused and several ) and carnivore . We alsoWe

ative of body mass - Hall 2008; specific specific

includ our and

- - Ursus life García García day day

, the

e

This article isprotected rights by All copyright. reserved. interactions between HPDAccepted and body mass HPD phylogenetic signal (lambda =0). between sp Using aphylogenetic generalized least squares approach account to patternsfor of relatedness lost all of their native aurochs and European bison bodymasses higher HPDs than larger species individual impacted species equally. original native Holocene large north andnorthwest Europe, with AD 2000 Holocene, with 209 recorded country ArticleHuman Results have contrasting high andlow HPDs and experienced cultural transitions HPD across the Holocene for two countries, UK and Norway, which are geographically proximate predictto the and lme4 (Bates et 2015)al. a All explanatory power Using the nalyses were conducted using the glm andglmer ( - 0.98 s

have major a been ofdriver losses of

( Figure 1; species’ CHPD and body ecies, we find the same slope and intercept theas simple linear regression andno clear , Figure below maximum continent

for

2 10 Data S ). ). European

explaining the influence of HPD andbody mass onmammal presence kg, T

- mammalian he model with highestthe explanatory value is wide We findWe a have 1: 1: Table , in R3.0.2.in

which - analysis bodied bodied populations . For example persisted areasin with

Britain, Denmark and

S have and patterns of

mass strong body - respectively. 3 level extirpations across 22 species from around 4000BC to mammal

) , we find an even stronger relationship between bodymass and (R Core Team 2017). . There wereThere a higher number of body masses

(Figure ( mass that see negative relationship , disappeared where , European Data S1: Table golden jackal and fauna

2 ), with), sm agri would be .

packages

However, human population pressures have not between 650 HPDs cultural intensification the Netherlandthe large mammal

W all greater than

able persistto

S e also used our MASS (Ve 4 er HPDs (

Eurasian otter for model comparisons - species 0. - 800 kg 61 were under 1

s population ± the onethe that

country all losing over

0.10, 100 able to nables andRipley 2004)

and which haveand which both now

at at different levels of

people at similar times continent , p <0.001 -

which both have level

tolerate substantially s

throughout the 0 includ /km people extirpations in 60% - ) 2 ) wide model . , whilst , whilst

es between The slope

/km -

of their absence. ,

but but 2 .

This article isprotected rights by All copyright. reserved. presentthe particularly low tolerance to human whilst presence, most small generally now regionally extirpated. Due to their survival through time for using long landscapes from least at the Mid popula Our study Discussion kg)(196 sizethe of its largest extant mammal species, e.g. European wolf ( model accurately predicts a bo Death was followed by particularly Norway show species that did include trophic level did not show any significant relationships of herbivory models therefore reduces the amount of scatter aroun theto fact that the for this model is steeper than the slope through the individual species regressions, likely attributable

Accepted dymass more than an order of magnitude higher than UK the due to its much smaller HPD. Article Our analysis of

in thein 14th century AD tions of large presence/absence. based on ,

and Eurasian elk (462 kg) excluded from - provide

term data archival onpast population losses we have been able to across substantial s

a marked decline across the Holocene for both countries

a small increase AIC fromthe inclusion of trophic level (

s much or all of their ranges despite escalating growth of human populations. W explicit

explicit evidence for ahistorical extinction filter that has selectively removed - the maximum bodied

reduction studies

Europe’s largest

inclusion bodyof mass incorporates greater explanatory powerand high mammal . By

-

of of extinction risk, but historical our analysis highlights their

sustainable mammalmass Norway for Holocene in sustainable body mass associated with AD 2000

mammalian body mass could that .

species with lower tolerances humanto presence from European absence from curren - bodied onwards ,

Norway could theoretically mammals sustain a with d the slope.

human population crash postglacial native , far earlier than has

We found nosignificant improvement our in Data S1: Table around 1000years ago, t - day European faunas,

er - Canis lupus bodied mammals, be sustained

in in the present day (Figure typically S

species resulting from 4 ). Similarly,). those models assess correlates of ; 32 ; kg), brown bear many 3

).

been been have in the and UK even though

t The UK suffered a

hese species are or or

of which of recognized survive carnivory

the Blackthe , including d O are

this

ur ur in e

on . to to

By

This article isprotected rights by All copyright. reserved. global anthropogenicof activity they exposed are to, and highlight extremethe vulnerability of large mammals particula in forecasts globalfor human population growth (Bradshaw human pressures either identifying nature of human societal develop can species strongthe statistical relationship between and temporally Neolithic 2011) and 2009al. species indirect mammals (Cardillo et al. 2005). which than smaller interl b humans across time space and than studies focused on the present time have Accepted Articleodymass and HPDthe at which a actually the development of scale H inked also also . umans have historically impacted mammal populations emphasiz - wilderness areas of low human density such for species However, /diseases, - wildlife interactionwildlife specific and continent ) processes .

onwards calculated and at regional spatial scales These processes would , highlighting that larger scenarios - represent bodied ,

es now and so

competition and/or the , including

that both intrinsic and extrinsic factors contribute towards extinction risk for larger (e.g

species thresholds of mammalian tolerance to human population or complex and staggered process of cultural where a reliable proxy for . Gkiasta et al. 2003)

are in in the future new technologies

. difficult to

This This particular even at hunting, - wide

study ment undoubtedly - mammal bodied mammalsbodied , low models

hybridization with domestic without necessarily requiring more detailed data on the

habitat loss/degradation . analyze mammal species are likely to be vulnerable , may be

Our analysis and thus have been able determineto finer prehistoric levels of HPD HPD across anthropogenic ,

means demonstrates that this general index humanof activity species becomesspecies regionally extirpated are strongly

directly relation in to mammal population losses have been accelerated by human population growth particularly and mammal population

the Holocene in Europe (Klein Goldewijk et al. provide support for

that these effects would have varied both spatially

may therefore constitute a useful tool have been

pressure and Brook useful and timely ,

through a

(Watson et al. 2016) and

and more vulnerable humanto activity

r r humans,to regardless of the type

mammal - , through time day alone

and other demic 2014)

the the importance of maintaining

support

loss range of processes s . diffusion

( Our . , Grayson 2001

given continued s We demonstrate shown both in our

over , despite the, despite complex ing

finding different

- to anthropogenicto

previous research scale responses to such such as . a millennial

from the s

also for direct and , Kaplan et introduced type of

that . Yet

This article isprotected rights by All copyright. reserved. kg both 2009)al. and local maintenance often persist highin at for the country heterogeneity HPD in and environmen predicted thresholds long and HPD, encouraging. highlights This the strength of the relationship precision associated with the of use and howthese interact with HPD. investigate more a specific series of life extinctions rather than may bedriving extinction patter biological characteristic which resolution of resolution for the purposes analysisof dataof become increasingly resolved well HPDs earliest possible mammalian millennial

Accepted (for Article - I Some mammal European do species currently survive countries in with HPDs above their remain term spatial and temporal ncorporating

derived from HYDE the database are HPD . For example, red deer ( - and scale historical data, , large

but last

widespread in the UK, of of 203 p our historical

supports increased use of

- these traits exhibit strong collinearity boundary date occurrence body mass - level spatial level spatial scale whichat we conducted our analyses baselines - . T elevation refugiaelevation eople his his of of populations of large “mismatch”

/ data km

has beenhas shown

records from long

2

is is extinction , , Figure 2 for which are inevitably somewhat imprecise

n w s Cervus elaphus highly

Nonetheless e chose to ( regional extinction rather than anabsolute

Woodward et al. 2005 where we predict historical data typically represent ; Fisher; 2011, Turvey 2015 al. et . tal tal characteristics such as topography - may be Similarly, term ecologicalterm archives requires the -

history traits associated with historical patterns of zooarchaeological and historical archives likely )

dyna ,

and but but

modeled to to keybe a focus on -

bodied bodied , g mics ( to due precise closer theto present, they are of acomparable these deer species

; 241 ; kg) androe deer ( iven the act as a because of sets primarily either to finer Turvey 2015; al. et

a estimates. (Johnson 2002). species species for conservation or hunting , claritythe the effects of body terminus post quem direct surrogate unavoidable issues of resolution and ) . For example, we detect mass threshold betweenof 3.6and the relatively broad temporal and spatial

driver of

However

are are heavily managed and consistency

for other key life body mass ), ), or between mammal extirpation F l uture research could

Capreolus capreolus ate Quaternary mammal Crees et 201 al. (

, because both . slow slow reproductive rate e.g. Our -

more recent scale scale regional dates, , which was not accounted

use use extinction remnant populationsremnant , a country of of

commonly

providing of of for for reconstructing centennial - history traitshistory that our

- (Ward 2005) level ma of these 6 date

results is ) (Dickson et . nagement extinction

- an

, therefore used used

; ; 23 kg) and - orscale 17.1 sets .

This article isprotected rights by All copyright. reserved. Accepted supportto populations of grazing andbrowsing herbivores populations intrinsically particularly v than from verified historical re former extinction filter. Indeed, relatively early extirpation, the highlybeen susceptible to extirpation by human large size trophic level mayspecies be better viewed asminimum estimates 99 the AD 2000in this country level. Articlepopulations historical scales orderin to 2014).al. recovery in some regionsof Europe, offsetting high human presence(Deinet et al. 2013, Chapron et active attempts to foster co low densities Pyrenees exclusively restricted to remnant populations montanein areas (e.g. severalin central European countries such as France, Switzerland, Austria and Italy, they are Likewise, although several large carnivores such wolf,as Although w th

Holocene large mammal as fauna, it centile of the HPD across their range at this date was used. As such, thresholds for these ) ,

and zooarchaeological

I where HPD is far lower many deally analysis our would ,

would be difficult if not impossible obtainto consistently across many species below vulnerable overharvestingto , and t

ulnerable to human pres e o It should also benoted that w ven ur ur study e found no additional rel formerlywidespread capture long heir in these high . Therefore, - dependence term term the European wild ass

more precise species - existence between people and wildlife have also facilitated mammal historical ports se - elevation regions

data are also paradoxically species the most likely to be subject to an

for species that e on than elsewhere in t (Crees and Turvey Large 2014). th

sures on patterns persistence of and extinction of different mammal primary productivitymeans analysis ungulate erefore , ationship between mammalian tolerance humansto and but but

for several reasons e only investigated mammalian extirpation and HPD up to is only known from t -

benefit from being undertaken at even spatial finer of of individual species has hey are a key hunting of target for food by human specific has been taxa s

in thein past

(Kaczensky al. et 2012). xperienced —

of tolerance to HPD. hese countries; however, in particularin Europe’s bovids HPD thresholds. Unfortunately largely brown

(Ripple et 2015)al.

(Figure :

no regional extirpations by this time, their slow reproduction render

forgotten as amember Europe’s of the zooarchaeologicalthe record bear and lynx ( that

the Alps,the Appenines and - 2 bodied ). ). large tracts landof

However, highlight

Legal protection and

ungulates are likely be to

. they A Lynx lynx ed

ny landscape due to due to the

and equids now that due to their ,

however, exist exist

) are required still ir almost s rather at

- —

them persist scale scale

very

have the

This article isprotected rights by All copyright. reserved. south (Eurostats 2019) a mammalsmay mixed be the long thresholds and growth extirpation example, coexistence with humans, results range human of subsistence uniformlybeen distributed through time space or changes in activity andpopulation moreinto direct conflict with humans (Bateman Fleming and 2012). predators suburban environments herbivores, some carnivores have more recently adapted to living the in margins of urban and habitat, or in areas unsuitable for maintaining large human populations elevations, specialists areas, Goldewijk et al changes are livestock, change Acceptedcross Article The Holocene is an important period Geographic variation in human demographic projections suggests that t and European ungulates show elevational niche differentiation between lowland and highland much of . In it could addition, aid identification of s, of of this study -

term absence the in of targeted conservation intervention including not only our with generalist diets will . By contrast,

and their ability prey to switch associated with either current

documented across Holocene Europe from early as as 1000 BC (Kaplan et al analysis therefore that . eastern

2010) have are therefore also relevant

could . ,

. However, and M and even r accumu across Europe educe food availability to support large ungulate populations, and such

ajor grassland andopen forest habitats also tend beto distr as

, central

the wide

help help to settlement well as large ,

and likelihood lated lated “extinction debts” - scale habitatscale loss and degradation

- demographics these carnivore species Europe bodied those that are identify species

responses , andpopulation density . H - day human population density future or

in uman population is , from Lithuania thein north Bulgaria to and Greece in the of of agricultural land abandonment ma carnivores can exploit a range of landscapes

human history, capturing y

to understandingto andmanaging

to humanto pressures also enable also them persist to marginalin and degraded

landscapes , larger and (Roberts

either Europe in or

or or populations of of species or populations that are unviable in are are almost exclusively 1998) m that expected ore ore

patterns continu

. However have already strictly ( in in Kuussaari et al. 2009 that ,

but but also historical populations. at at a extensive and

(Ripple et 2014)al. to may carnivorous tend cometo global decrease ,

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scale

to exist today. medium human changes

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- 2009; Klein

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This article isprotected rights by All copyright. reserved. evidence extent of past human impacts onglobal mammal faunas importance of using long thresholds for extinction continental scale extensive understand how define populations bodied modern conservation action that can reverse negative effects human of reintroduction species rewilding high human density by 2050, the countries ~ associated pressures opportunities for further largemammal recovery these regions ( 25

Accepted Articlese countries are also expected to - ly populated 50% in areas in 50% of western andnorthern Europe such Britain as Our I

nformation onnformation

the negativethe mammals have historically extremely been vulnerable evento relatively low human -

study highestthe base t base (Eurostats 2019) new ,

and Perpiña Castillo

sites (Seddon al. et 2014). dataset of mammalian to uniquely hat will help protect to

larger ,

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, countries. urb we

and relationship between

historical (Deinet et al. 2013). By contrast, human populations are projected to increase proportion an spaces may therefore alleviate pressures on introduce - in thein absence of to bodied

uses across a wide range mammal of - anticipate the likelihood term historical and even prehistoric datasets to better understand the full , potentially increasing human

an

HPD thresholds species

et al. 2018) s a

empirical n analytical in Europe have over 90% of regional extirpations

are increasingly vulnerable threatened

technologi

species body mass tolerance and HPD, to The use of past data also highlights that thein absence of . l

ate (United Nations 2018) Th

framework ese projectedese changes Quaternary may

in in the face declining of human populations popu of of survival for different speci cally advanced hunting methods

also be be also their lations ,

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in orderin to taxa m

across the data ammal encountersammal and conflict human populations living urban in areas useful

can

. into the future

These findings highlight - driven approach identify ,

. to humanto impacts. in in Scandinavia The The

large mammal contribute to targeting could entire Holocene Epoch - wildlife wildlife interaction, large shift in

species

present .

suitable , and Benelux the concentration of es es within

- to

specific a

s

. to betterto multiple conservation demonstrate even in

Using landscapes

the the

proposed HPD ; however; an the mostthe

and and at a

and -

for , This article isprotected rights by All copyright. reserved. Brook, B. D. W.,and M. Bradshaw, C. and B.J., W. Brook. 2014.Human population reduction is not aquick for fix Bojarska, K., and N.Selva. 2012. Spatial patterns brownin bear Benecke, N.1999, The Holocene history the of European vertebrate fauna: modern aspects of Bates, Bateman, P.W. Barnett, R., N. Yamaguchi, I. and A.Cooper. Barnes, 2006. The origin, current diversity and Ballari, S. Arnold, J., A.Humer, M.Heltai, D. Murariu, N. Spassov, Hacklaender. andK. 2012. Current status References Royal Society University Research Fellowship (UF080320 a and (NE/G011745/1) Grant Council Research Environment Natural a by provided was Funding Acknowledgements lme4. J Statlme4. J Softw 67 287:1 conservation of modernthe lion ( affecting food selection in native introduced and ranges. Mamm and distribution of golden jackals Acceptedprehistoric and modern body size environmental problems. Proc Natl Acad Sci geographical and environmental factors. Mamm research: Archäologie Eurasien,in Bd. Rahden/Westf., Verlag MarieLeidorf GmbH Article

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This article isprotected rights by All copyright. reserved. AD. Predicted mass wascapped at 1000 kg and Norway (blue line and points) using estimated human densities population from 8000BC 2000 to Figure was excluded from analysis interactions between HPD and body mass given by full the species thresholds values are logged. shown curves ( s Figure AD 2000. sustainable body mas Figure 1. Zuo, W.,F.A. Smith, and E. L. Charnov. 2013. A life E.Wright, pecies Accepted Articlemegafaunal extinction. aurochs ( 3 for species 2

against body mass (kg) ( Data S1: Table . .

N Predicted Individual estimates of critical human , Bos primigenius

umber of species and S. Viner

continent

that g Solid

maximum

s (kg)

(±95% CI) have experienced no recorded country S - 2 Daniels. 2015.Daniels. Geographical variation in sizethe and shape of Europeanthe Am Nat182:524 rey ) - . ). J Arch ). J Sci 54:8 wide analysis

(right (right plot) (see Estimated

(left plot) line body massbody thresholds (kg) for black

Methods . Dotted

and band

points ; u

for each European country human population density (N/km2) pper (99

including all presence . ). grey -

531. The wildcat (

. represent

) -

22. calculated using receiver operating characteristic (ROC) line line represents

population th

centile) a - history approachhistory theto late Pleistocene simple Felis

human density the United Kingdom (red line and points) - ) was) an outlier

level the the

linear regression - absence data optimum population densities at AD 1, AD 1000, AD 1500and

(N/km extirpat 2

ions

±95% CI)±95% of general linear model (middle plot);

(open circle point) and incorporating

( fit fit through grey points at AD 2000

22 maximum

individual mammal ).

All All fit fit and

This article isprotected rights by All copyright. reserved. Accepted Article

This article isprotected rights by All copyright. reserved. Accepted Article

This article isprotected rights by All copyright. reserved. Accepted Article