Osteological comparisons of appendicular skeletons a casestudy on Patagonian huemul deer and its implicationsfor conservation

Werner T FlueckABC and Jo M Smith-FlueckB

ANational Council of Scientific and Technological Research (CONICET) Buenos Aires Swiss Tropical InstituteUniversity Basel DeerLab CC 592 8400 Bariloche Argentina

BInstitute of Natural Resources Analysis ndash Patagonia Universidad Atlantida Argentina CC 5928400 Bariloche Argentina

CCorresponding author Email wtfdeerlaborg

Abstract Early explorers described huemul (Hippocamelus bisulcus) as stocky massive and short-legged deer ofmountains comparing them to ibex (Cabra ibex) chamois (Rupicapra rupicapra) mountain sheep (Ovis canadensis)and mountain goats (Oreamnos americanus) Subsequent key paleontological work also claimed that huemul are mountaindeer However all these comparisons of huemul to other ungulates were done without any supporting data These historicevents lead to (i) the continued prevailing claim that huemul aremountain deer and (ii) that their natural range is theAndeanmountains as evidenced by the current distribution We found that early writings about huemul generally reported theirrareness disappearance or near extinction References to stocky and short-legged huemul were casual remarks made aboutdeer found mainly in refuge areas Paleontological comparisons were based on a new fossil labelled as mountain deerwhich however has been shown to be a construct and declared a lsquonomen nudumrsquo Behaviour like the aggressive horseshoestance and thick long hair dissimulate stockiness by distorting body shape Comparing leg morphometrics of huemul and12 other ungulates revealed that huemul cannot be associated with rock climbing species Intraspecific proportional leglength is not static and is influenced by ecogeography nutrition physiology and factors affecting exercise Thus climatealtitudinal hypoxia and locomotor pattern employed according to terrain predation and forage affect the appendicularskeleton Nutritional deficiencies occurring in Andean mountains are notorious for affecting bone development causingosteopathology and altering body shape Frequent underdeveloped huemul antlers and high incidence of osteopathologysupport the effect from mineral deficiencies Skeletal proportions are affected by numerous factors causing largeintraspecific variation Relative metapodial length varies up to 70 in better studied cervids and populations fromdifferent environments can be clearly distinguished Huemul morphology does not overlap with rock climbing speciespreviously considered analogous but falls within the range of other cervids We caution against the rigid application ofmodern huemul occurrences in interpreting past habitat use The few historic extra-Andean accounts cannot be consideredabnormal outliers Huemul ecology must be interpreted in terms of first principles rather than applying direct analoguesfrom the present This allows us to begin to use the past to understand the present instead of repeating the fallacy of imposingthe present on the past Current efforts to recover remaining huemul are distinctly based on the assumption that huemulforemost belong in ruggedmountains because of their supposed special adaptions and resemblance to stereotype ungulatesalso erroneously believed to only occur in ruggedmountains elsewhereWe conclude that the present empirical comparisonssupport many other lines of evidence that huemul existed in treeless habitat and colonised Andean forests and higheraltitudes secondarily Habitat breath of huemul is thus more like that found in other closely related Odocoilines promisingtremendous new opportunities for recovery efforts

Additional keywords adaptation epigenetics Hippocamelus bisulcus morphometry skeletal ratios

Introduction

Early European explorers and naturalists described huemul(Hippocamelus bisulcus) as stocky massive and short-leggeddeer of mountains comparing them to ibex (Cabra ibex) andchamois (Rupicapra rupicapra) in their homelandTheyassumedhuemul to be a mountain deer just as was the interpretationof ibex and chamois at that time ungulates which by thenwere mainly surviving in remote alpine areas Similarly North

American workers compared huemul to mountain sheep (Oviscanadensis) and mountain goats (Oreamnos americanus) Morerecent authors1ndash6 often referring to these early writings makesimilar statements Although Diaz showed already in 1993 howhistory erroneously lsquoled to the assumption that the huemul was adeer of the mountains and that it had always inhabited areas inproximity to rugged topographyrsquo7 the importance has remainedlargely unrecognised and the paper mentioned only a few times

CSIRO PUBLISHING Review

wwwpublishcsiroaujournalsan Animal Production Science 2011 51 327ndash339

CSIRO 2011 101071AN10174 1836-093911040327

in passing Moreover huemul being a mountain deer is oftenreiterated and supported by referencing key paleontologicalwork a study which however was erroneous (see below)Problems with interpretations based on nonmetric traitsinclude high degrees of inter- and intraobserver subjectivity ofqualitative descriptions and thus proneness to false dichotomiesMain results of these historic influences are 2-fold by fomentingpersisting claims that (i) huemul are mountain deer specialisedto rugged terrain and (ii) that their natural range are the Andesmountains as evidenced by the current distribution evenwhile acknowledging the currently reduced and fragmenteddistribution

Current efforts to recover remaining huemul subpopulationsare distinctly based on the assumption that prevailing ecologicalinterpretations of huemul are correct despite a recent reviewshowing that even the basic ecology is little known orunknown8 The evolutionary history of huemul has majorimplications for the prospects of successful species recoverywhich so far has failed Evolutionary history is preferablyevaluated having some reliable parameters for inference ofadaptations for locomotion as more vague intuitiveinferences based on overall similarities and phylogeneticaffinities are often not applicable The functional morphologyof mammalian postcranial remains can be used to inferlocomotor adaptations and by association habitat relationsAll references we have found comparing huemul to otherungulates have been statements without any supporting dataWe analysed various observations and assumptions related tohuemul body shape and its relation to adaptations to mountainsand compared huemul to other ungulates with the objective todetermine if huemul can justifiably be considered a mountainspecialist and if not to describe the relation of its morphology toavailable habitat

Methods

We review past and more recent claims of huemul being stockymassive and short-legged and living principally in high Andeanmountains analyse phylogeny particularly with regards to theonly empirical paleontological work from which huemulreceived the vernacular name lsquomountain deerrsquo and reviewbehavioural and physical aspects of huemul contributing to theappearance of stockiness

Weprovide thefirstmorphometric analysis of leg bones fromhuemul based on complete leg assembliesMeasurements (mm)taken with calipers were recorded for total length articularwidth and width (lateral) and depth (antero-posterior) ofshafts at the most narrow section Circumference wasobtained with a flexible tape measure Samples stemmedfrom Chile (Punta Arenas) and Argentina (province of RioNegro specimens cmhp316 and 345 province of ChubutCITES permit No 020729 permits 3706 3806 and 0307issued by the Direccioacuten de Fauna y Flora Silvestre andNationalParks permit 91508)

Data from huemul were compared with other ungulatesNavahoceros9 Odocoileus lucasi10 mule deer O hemionus1112

ibex1314 chamois measured in Basel NaturhistorischesMuseumSwitzerland specimennumbersCIII386C3607C3667C728729 C9635 C2279 and1213 tahr Hemitragus jemlahicus

measured in Basel Naturhistorisches Museum specimennumbers 10 753 and13 Marco Polo sheep Ovis ammon13

bighorn sheep O canadensis1315 mountain goat1213 red deerCervus elaphus our collection from Patagonia and12 and blackantelope Antilope cervicapra13 Finally factors which are knownto affect body proportions are summarised

Results

Initial written accounts on huemul can only be understoodcorrectly by acknowledging the concurrently reported rarenessor reference to being already endangered Most early observersnoted the already unnatural state and remarked that huemul wererare disappearing and becoming extinct eg 185716 189717

191018 193519 194120 194621 194922 196823 In 1929 theChilean government made a law providing total protectionand in 1932 the Argentine government employed a Germanscientist to start a breeding station aimed at avoiding extinctionof huemul24

References to stocky massive and short-legged huemul

According to Krieg in the 1920s huemul in Argentina remainedonly in remote areas hiding in brush above the treeline whereasonly very few people living on the western side of the Andeshad seen huemul although they had lived there for manydecades25 He also noted the very thick fur comparing it tomountain goats and compared the hind legs to those of chamois acomparison also made by Kolliker Frers26 In 1897 Heckcompared appearance and behaviour of Hippocamelus toibex27 Then in Kurtenrsquos28 technical paper Hippocamelus wasreferred to as mountain deer based on (unquantified) short legsbeing related to the ancestral cervid Navahoceros andcomparable to ibex and chamois More recently huemul weredescribed aswell adapted to broken difficult terrainwith a stockybuild and short legs (2930 httpwwwwikipediaorg httpwwwambientegovar verified 21 January 2011) or as havingvery short legs and found in rugged terrain and steep slopes of theAndes (httpwwwarkiveorg verified 21 January 2011)Eisenberg1 also considered huemul a typical high-altitude formby claiming that body proportions lsquoare reminiscentrsquo of bighornsheep (however no data provided) appearing to occupy a similarniche as bighorn sheep Argentine governments and NationalParks (31 httpwwwambientegovar) and recent natural historyaccounts245 concur with his statements that huemul have arestricted distribution exclusively inhabiting the forests andsub-Andean grassland of the Patagonian Andes and are short-legged Clearly since the first descriptions of remnant huemulgroups right up to the present huemul has foremost beenconsidered a mountain deer based on subjective descriptionsof physiognomy and distribution in recent times

Evolutionary phylogeny

Kurten9 describing a new fossil North American cervidNavahoceros fricki pointed out its lsquohighly unusual adaptivecharactersrsquo among cervids specifically referring to very thick-set limb bones short metapodials and simple antlers Providingleg bone measurements of this fossil he interpreted the sizesas extreme adaption to mountains thereby applying the common

328 Animal Production Science W T Flueck and J M Smith-Flueck

name lsquomountain deerrsquo for Navahoceros Further he stated thatthe plump limb bones are reminiscent of those from alpinechamois and ibex claiming them to be adaptations to analpine rock climbing mode of life He contrasted Navahocerosto another fossil deer which he had described as Sangamonaa long-legged deer located east of the former28 thus reenforcinghis new lsquomountain deerrsquo Navahoceros He made the explicitcorrelation that Hippocamelus was related to Navahoceros onlydiffering by having two instead of three antler tines28 he thusconsidered Hippocamelus implicitly to be homologous tochamois and ibex Subsequently Webb32 looked at one partialcranium of Navahoceros to interpret phylogenetic relationshipsReferring toKurtenrsquos9 interpretationofNavahoceros asmountaindeer he further stated that lsquoclearly Navahoceros shares withHippocamelus very short metapodialsrsquo however withoutoffering data or references and that lsquothe correlation of skeletalproportions with mountain habitat is certainrsquo again without dataor references Later on NewWorld cervids Webb33 reconfirmedclose cranial relationships between Navahoceros andHippocamelus reiterated the very short metapodials of bothand concluded that soon after the Panama land bridge wasestablished this lineage of lsquomountain deerrsquo being betteradapted to the high Andes thus became established thereWebb reiterated (2007 pers comm) lsquothat the North Americanmountain deer Navahoceros was phylogenetically affiliatedwith Hippocamelus but surely could not have remainedrigidly tied to alpine settings if during the Plio-Pleistocenethey extended their range through the isthmian regionrsquoClearly immigration of temperate species from North Americawas filtered through a subtropical-tropical barrier34 Regardlesshuemul continued to be claimed to be lsquomountain deerrsquo based onancestral Navahoceros which contributed to further reenforcingcontemporary claims that the current remnant populations inhigh elevation central Andes are there and have survivedbecause it is their prime habitat

However a necessary closer look at Kurtenrsquos original paper9

reveals major methodological flaws For example no standarddeviations on leg bone measurements (n = 9ndash52) of N frickiwere provided nor any indication as to sex or age Thushis averages cannot be interpreted being well known thatage and sex influence the size of leg bones in dimorphicungulates14 Furthermore bones in the consulted multi-species collections are disarticulate individual bones notcomplete sets of legs and mixtures of ovids and cervids areprone to be confused (CDailey pers comm)AsKurten did notprovide collection identification numbers it was impossibleto duplicate his work10 For comparisons Kurten referred tomeasurements taken on only one single O hemionus withoutproviding the origin sex nor age Notably this specimenwas near the extreme of long-leggedness for this species(metatarsalfemur = 097) compared with the reported range(082ndash100)1112

The most comprehensive analysis of fossil records pertainingto origins of huemul was provided by Morejohn and Dailey10

which was based on detailed descriptions of new completefossil finds reconfirming the ancestral form O lucasi as aNorth American endemic species In addition a painstakingreanalysis of many museum collections particularly the onesconsulted by Kurten was summarised as follows

(1) All bones labelled as Navahoceros and all skeletons invarious museums assembled from piles of disarticulatedbones were confirmed to be Odocoileus

(2) N fricki is considered a lsquonomen nudumrsquo and(3) Sangamona fugitiva was also confirmed to be Odocoileus

Sangamonawas declared a nomen nudum already in 198435

as a construct of diverse and disparate skeletal elements allof which derive from other and usually better known taxaand except in the minds of men never existed

Thus N fricki and lsquomountain deerrsquo have been invalidatedand the focus remains on O lucasi as ancestral form forHippocamelus Another fossil species O brachyodontusrecently shown to fall within the variation of other Odocoileuswas also declared lsquonomen nudumrsquo36 ThusO lucasi remains thelikely primary link to Hippocamelus

Behavioural and physical factors affecting huemulbody shape

Huemul at a glance can appear stocky and short-legged especiallymales For one a peculiar behavioural trait portrays a stancewhichdistorts body proportions Huemul appear naturally unafraid ofhumans since they frequently do not run or even walk away whenapproached allowing people to get extremely close (Fig 1a)37

Such curiosity and apparent lack of fear in approaching humans isalso known for several other ungulates includingmountain goats38

and bighorn sheep39 Nevertheless Povilitis29 first described anaggressive posture of huemul at close range when first alarmedhuemul remain still and keep the front legs parallel and inclinedposteriorly and hind legs in a forward position (Fig 1b)We positthat this stance is a homologous behaviour to that called thehorseshoe posture which involves shifting of the back hoovestowards the front hooves with the legs now forming a trianglewith the abdomen According to Cowan and Geist40 it involves ahunched posture with flexed hind legs having the effect oflowering the height of the animal The flexure of the hind legsis greater than that of the forelegs resulting in an arched back andlow-rumped position leading to the impression that the animal isstocky and short-legged This aggressive behaviour is commonamong Capreolinae41 such as Alces alces42 Rangifer tarandus41

Odocoileuswithmost exaggeration in periglacialO h sitkensis40

and huemul (Fig 1b) but also occurs in mountain goats38

A further feature adding to apparent stockiness and shortlegs is related to the thick hair coat which in winter providesthermoneutrality down to 50C43 This results from a densewooly underfur keeping the 7ndash9-m-long hair straight44 Theappearance of a shedding huemul has repeatedly beencompared with sick animals as hair comes out in clumpssimilar to other mammals from cold climates The extremelythick hair coat thus contributes substantially to the perceivedstockiness of huemul (Fig 1c)

Morphometrics of huemul and other ungulates

Although a shaved huemul would be instructive to revealmusculoskeletal relationships body proportions can also bededuced from bone measurements (Table 1) Data from adultmales were encountered more frequently and huemul bucks alsoprovided the largest set of complete leg assemblies

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 329

Interspecific proportional appendicular bone lengths werecompared by standardising femur length (Table 2) Arrangingmetatarsals according to their proportional length as the mainindicator of locomotor use13 there is a clear groupingof ungulates

living in extreme steepness and rockiness (lsquotrue rockclimbersrsquo15) followed by species merely potential lsquoinhabitantsof rocky areasrsquo like bighorn sheep or chamois to black antelopeconsidered to be the fastest running ungulate45 The widely

(a)(b)

(c)

Fig 1 (a) Huemul unaccustomed to humans frequently have very short flight distances (photo by J M Smith-Flueck) (b) The aggressive stance of huemul atclose range known as the horseshoe posture (c) The 7ndash9-cm-thick hair coat is best appreciatedwhen being shed (courtesy ofGGaray) Note in the left photo thatthe diameter of the upper neck is substantially less than further down in the unshed portion

Table 1 Lengths and articular width (mm) of appendicular bones from adult male and female huemul

Males Femalesn Length sd Distal sd Proximal sd n Length sd Distal sd Proximal sd

Humerus 7 237 69 472 16 65 31 2 217 43 508 106Radius 10 214 53 40 15 41 09 4 205 47 40 37Metacarpus 12 172 43 37 05 35 07 4 163 40 325 31

Femur 11 276 54 715 15 65 23 4 257 81 534 143 585 071Tibia 16 315 103 433 12 64 19 8 294 86 407 149 62 183Metatarsus 13 201 71 37 07 33 12 5 192 21 355 105 311 146

330 Animal Production Science W T Flueck and J M Smith-Flueck

accepted rock specialists (mountain goats ibex tahr) are clearlyfar different even from bighorn sheep Speedy Black antelope onthe other extreme are also separated distinctly by proportionallymuch longer metatarsals

Among ungulates the tibia femur and radius humerus ratiosare rather uniform and corroborate that differences in legproportions relate mainly to metapodials1346 (Fig 2a) Amongspecies compared here (Table 2) standardised tibias varied byonly 47 whereas the metatarsals varied by 196 Alsoproportions between segments of the hind leg are very similarto those of the front leg in the same individual Asmetapodials areimportant for gait dynamics Table 2 shows the tibia metatarsalratio among ungulates A larger ratio means that metapodials areshorter and the pattern largely coincides with proportionalmetatarsal length Again the group of lsquotrue rock climbersrsquo hasthe largest tibia metatarsal ratios

Stoutness refers to bone length in relation to thickness orarticular width with smaller ratios indicating stouter bonesStout bones are the physiological reaction to forces and wouldgo in parallel with larger muscle masses Table 3 presents theratios of appendicular bone length in relation to articularwidth Huemul are compared with ibex (lsquotrue rock climberrsquo)and red deer as originating from steppes47 Out of the 12possibilities (six leg bones middot two ends) huemul only once hadthe stoutest yet three times the least stout articulate endsRemarkably ibex were stoutest and red deer the least stoutfor all metapodial ends (Table 3) Additionally in true rockclimbers tibia are the longest bone and metatarsals range fromjust over to just under half of tibial length15 again placinghuemul far from true rock climbers (Table 4)

Finally bone circumference as a measure of bone strength ishighly correlated with body mass in bones primarily supporting

Table 2 Proportional length of appendicular bones from various ungulates using the femur for a standard length (arranged according tometatarsal length)

Mountaingoat

Ibex Tahr Bighornsheep

Huemul Navahoceros Chamois Ovisammon

Tuleelk

Muledeer

Odocoileuslucasi

Reddeer

Antilopecervicapra

Femur 1 1 1 1 1 1 1 1 1 1 1 1 1Tibia 109 116 111 118 114 107 126 118 119 115 110 114 123Metatarsus 048 057 057 070 073 079 079 079 080 082 084 085 101

Tibiametatarsus 227 204 195 169 156 114 159 149 119 140 131 134 122

n 3 26ndash32 6 2 11ndash16 9ndash52 7 15 1 1 1 2 4Sex Male Male Mixed Unknown Male Unknown Male Male Unknown Unknown Male Male Mixed

100

10 000

circumference humerus79 species

79 species

circumference radius

male huemul (n = 3)

male huemul (n = 3)

1000

1000

100

1010 100 1000

Body mass (kg)

Body mass (kg)

Dim

ensi

on (

mm

)D

imen

sion

(m

m)

Weight (kg)

cm

10 000

100

1010 1000100 10 000

90

80

70

60

50

40

30

20

10

020 40 60 80 100 120 140 160

Hindleg

tibfemur

(a)(b)

Fig 2 (a) Tibia femur ratios among ungulates mentioned in the text in relation to leg length and arranged according to bodyweights (46 huemul from presentstudy) (b) Bone circumference in relation to body mass in 79 different species analysed by48 and adult male huemul from the present study

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 331

body mass such as femur tibia humerus and radiusMeasurements on forelegs of three adult male huemul coincideclosely with correlations among 79 species analysed byChristiansen48 (Fig 2b)

Factors affecting body proportions

Constraints regarding body proportions are set by geneticshowever intraspecific variation is due to adaption followingecogeographical rules nutritional and physiologicallimitations4950 According to Flueck51 skeletal muscles areextremely plastic in their capacity to remodel according toalterations in physical demands such as in response to averageneeded muscle work as a function of terrain disturbances andfood density As most species fill the landscape along the fullspectrum of habitat qualities from source to sink areas bodyshapewill varywithin a species52 Scott53 observed that cervid leglong bones are highly variable depending on habitat usedpredator avoidance strategy used gait and locomotor patternemployed It is the distal limb segments (metapodials)however which undergo more length modification thanproximal segments121354ndash56

A most relevant ecogeographical pattern known since 1877Allenrsquos rule is found between climate and morphology as athermoregulatory adaptation This principle explains changes inratios of body surface area to body mass in hot and cold climatesand predicts short and broad limb proportions for animals incolder climates For instance bighorn sheep in cold climate haveshorter legs than bighorns in warm deserts57 Besides ampleempirical cases adaptions were shown experimentally in pig

litter mates raised at 35 20 and 5C (Fig 3a)58 or rats raised at28 and 5C54 colder temperature resulted in increased hairdensity and stockiness and shorter proportional leg lengthFurthermore oxygen pressure has also been recognised toinfluence bone growth With higher altitude increasinghypoxia results in reduced growth of distal limb bones alreadyat the fetal stage and thus proportionally shorter legs5960

Certain nutritional factors play well known roles in shapingbody proportions Iodine deficiency affects bone growth bydecreasing muscle function and thereby affecting boneremodelling and by direct effects on bone growthmetabolism506162 including shortening of metapodials andjoint disease6364 cretinism in its worst form including insheep and deer65 Selenium deficiency has a synergistic effectand produces shorter bones and overt osteopathology like Kasin-Beck disease6667 Andean mountains are deficient in iodine andselenium and may relate to high incidences of suchosteopathology in huemul68ndash70 Similarly a high prevalence ofosteoarthritis has been noted in moose (A alces) which wascorrelated with shorter metatarsals from nutritional constraints71

Corroborating trace mineral deficiency in huemul is the punyantler developmentnoted inmany remainingpopulations70whenconsidering the clear relationship between such deficiencies andreduced antler growth in other wild Odocoilines72

Discussion

lsquoMountain deerrsquo remains as a misconception about huemulIt originated from early explorers stressing the resemblance toibex chamois mountain sheep and mountain goats Howeverearly on huemul were described as rare and endangered andmany observations came from remote Andean refuge areas Inaddition the peculiar aggressive behaviour of huemul thehorseshoe posture and the very long hair coat may give animpression of stockiness These early casual statements aboutbody shape were later reenforced by key paleontological worklinking huemul to the fossil lsquomountain deerrsquo Navahoceros9 Thiswas an unfortunate error since the fossil was later shown to bea nomen nudum and corresponding to ancestral O lucasi10

Kurten also stated that huemul differed from Navahoceros byhaving two and not three tines on the antlers yet huemul haveup to five points673 Strikingly all of Kurtenrsquos comparisons tohuemul were also done only as casual statements withoutsupporting data yet his Navahoceros continues to enterphylogenetic interpretations323374

Thepresentmorphometric analysis shows for thefirst time thathuemul appendicular morphology is completely different fromthat of ungulates considered true rock climbers Thus neither theproportional metapodial lengths nor tibia metatarsal ratio normeasures of bone stoutness have any resemblance to rockclimbers Although bighorn sheep or chamois are consideredat times as lsquoinhabitants of rocky areasrsquo15 this applies equally wellto red deer7576 and even to American bison (ie lsquomountainbuffalorsquo) which lsquoused precipices so steep that hunters could notfollow them and even for dogs it was doubtful if they could havefollowed unharmedrsquo77 In little time exotic red deer haveinvaded all habitat types used now and in the past byhuemul78 confirming that both species can equally occupyAndean habitat types In fact of all species considered in this

Table 3 Comparison of stoutness among huemul ibex and red deerratios of appendicular bone length to articular width at distal and

proximal ends

Ibex Huemul Red deer Comparative stoutnessMaximal Minimal

Lengthdistal articular widthFemur 481 385 347 Red deer IbexTibia 85 727 897 Huemul Red deerMetatarsal 43 543 683 Ibex Red deerHumerus 485 502 467 Red deer HuemulRadius 474 535 559 Ibex Red deerMetacarpal 364 465 625 Ibex Red deer

Lengthproximal articularwidthFemur 406 423 363 Red deer HuemulTibia 5 492 461 Red deer IbexMetatarsal 526 609 699 Ibex Red deerHumerus 367 365 334 Red deer IbexRadius 46 522 497 Ibex HuemulMetacarpal 405 491 607 Ibex Red deer

Table 4 Percentage difference between half the tibial and totalmetatarsal lengths as an indication of affinity to a true rock climber15

Mountain Ibex Chamois Bighorn Huemul Redgoat sheep Male Female deer

+155 +21 ndash235 ndash27 ndash276 ndash307 ndash56

332 Animal Production Science W T Flueck and J M Smith-Flueck

paper those with proportional metatarsal length of 07ndash085(Table 2) are all well known to successfully inhabit rockyareas Instructively bighorn sheep and all species with longerproportional metapodials including chamois huemul and muledeer (Table 2) are also found in flat open areas Bighorns arewell known to inhabit or have inhabited low flat deserts andgrasslands7980 and sheep in general can do without rocks orcliffs Similarly chamois as an lsquoalpinersquo species is an artefact ofpast human-induced displacements81 since remains have beenfound down to near sea level82ndash84 as well as in rolling forest-coveredhillswhich they currently repopulate rapidly (nowcalledlsquoforest chamoisrsquo)8586 Lastly even Alpine ibex is a misnomer

extermination was much easier and much earlier at low andmedium altitude resulting in a prejudice in earlier years byreintroducing them to high elevations because that was wherethe last remaining groups were known from87 Recognised onlyrecently these reintroductions have actually created anartificial model of an animal of high altitude living there in allseasons above the tree line87ndash89 In contrast paleozoological datanow indicate that ibex occupied many additional topographicpositions than they do today89 Although ibex may remain inareas with some cliffs many fossils have been found down tosea level sometimes as dominant prey species in archeologicalsites and altitude clearly was not a factor in ibex ecology88 At

110

100

90

80

70

60

50

40

2 4 6 8 10 12

Species

Met

atar

sus

fem

ur (

)

14 16 18

1 data point

Lower limit

Upper limit

(a)

(b)

Fig 3 (a) Body proportions of pig litter mates raised at 35 and 5C fed to the sameweights58 (b) Intraspecificvariation in proportional leg length among several ungulates Sources are listed in Table 5 The species aremountain goat (1) tahr (2) ibex (3) Odocoileus virginianus (4) Rangifer tarandus (5) Bighorn sheep (6)huemul (7) Ovis dalli (8) Navahoceros (9) Ovis ammon (10) chamois (11) red deer (12) Dama dama (13)Odocoileus hemionus (14)O lucasi (15)Capreolus capreolus (16) Antilocapra americana (17) andAntilopecervicapra (18)

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 333

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

Interspecific proportional appendicular bone lengths werecompared by standardising femur length (Table 2) Arrangingmetatarsals according to their proportional length as the mainindicator of locomotor use13 there is a clear groupingof ungulates

living in extreme steepness and rockiness (lsquotrue rockclimbersrsquo15) followed by species merely potential lsquoinhabitantsof rocky areasrsquo like bighorn sheep or chamois to black antelopeconsidered to be the fastest running ungulate45 The widely

(a)(b)

(c)

Fig 1 (a) Huemul unaccustomed to humans frequently have very short flight distances (photo by J M Smith-Flueck) (b) The aggressive stance of huemul atclose range known as the horseshoe posture (c) The 7ndash9-cm-thick hair coat is best appreciatedwhen being shed (courtesy ofGGaray) Note in the left photo thatthe diameter of the upper neck is substantially less than further down in the unshed portion

Table 1 Lengths and articular width (mm) of appendicular bones from adult male and female huemul

Males Femalesn Length sd Distal sd Proximal sd n Length sd Distal sd Proximal sd

Humerus 7 237 69 472 16 65 31 2 217 43 508 106Radius 10 214 53 40 15 41 09 4 205 47 40 37Metacarpus 12 172 43 37 05 35 07 4 163 40 325 31

Femur 11 276 54 715 15 65 23 4 257 81 534 143 585 071Tibia 16 315 103 433 12 64 19 8 294 86 407 149 62 183Metatarsus 13 201 71 37 07 33 12 5 192 21 355 105 311 146

330 Animal Production Science W T Flueck and J M Smith-Flueck

accepted rock specialists (mountain goats ibex tahr) are clearlyfar different even from bighorn sheep Speedy Black antelope onthe other extreme are also separated distinctly by proportionallymuch longer metatarsals

Among ungulates the tibia femur and radius humerus ratiosare rather uniform and corroborate that differences in legproportions relate mainly to metapodials1346 (Fig 2a) Amongspecies compared here (Table 2) standardised tibias varied byonly 47 whereas the metatarsals varied by 196 Alsoproportions between segments of the hind leg are very similarto those of the front leg in the same individual Asmetapodials areimportant for gait dynamics Table 2 shows the tibia metatarsalratio among ungulates A larger ratio means that metapodials areshorter and the pattern largely coincides with proportionalmetatarsal length Again the group of lsquotrue rock climbersrsquo hasthe largest tibia metatarsal ratios

Stoutness refers to bone length in relation to thickness orarticular width with smaller ratios indicating stouter bonesStout bones are the physiological reaction to forces and wouldgo in parallel with larger muscle masses Table 3 presents theratios of appendicular bone length in relation to articularwidth Huemul are compared with ibex (lsquotrue rock climberrsquo)and red deer as originating from steppes47 Out of the 12possibilities (six leg bones middot two ends) huemul only once hadthe stoutest yet three times the least stout articulate endsRemarkably ibex were stoutest and red deer the least stoutfor all metapodial ends (Table 3) Additionally in true rockclimbers tibia are the longest bone and metatarsals range fromjust over to just under half of tibial length15 again placinghuemul far from true rock climbers (Table 4)

Finally bone circumference as a measure of bone strength ishighly correlated with body mass in bones primarily supporting

Table 2 Proportional length of appendicular bones from various ungulates using the femur for a standard length (arranged according tometatarsal length)

Mountaingoat

Ibex Tahr Bighornsheep

Huemul Navahoceros Chamois Ovisammon

Tuleelk

Muledeer

Odocoileuslucasi

Reddeer

Antilopecervicapra

Femur 1 1 1 1 1 1 1 1 1 1 1 1 1Tibia 109 116 111 118 114 107 126 118 119 115 110 114 123Metatarsus 048 057 057 070 073 079 079 079 080 082 084 085 101

Tibiametatarsus 227 204 195 169 156 114 159 149 119 140 131 134 122

n 3 26ndash32 6 2 11ndash16 9ndash52 7 15 1 1 1 2 4Sex Male Male Mixed Unknown Male Unknown Male Male Unknown Unknown Male Male Mixed

100

10 000

circumference humerus79 species

79 species

circumference radius

male huemul (n = 3)

male huemul (n = 3)

1000

1000

100

1010 100 1000

Body mass (kg)

Body mass (kg)

Dim

ensi

on (

mm

)D

imen

sion

(m

m)

Weight (kg)

cm

10 000

100

1010 1000100 10 000

90

80

70

60

50

40

30

20

10

020 40 60 80 100 120 140 160

Hindleg

tibfemur

(a)(b)

Fig 2 (a) Tibia femur ratios among ungulates mentioned in the text in relation to leg length and arranged according to bodyweights (46 huemul from presentstudy) (b) Bone circumference in relation to body mass in 79 different species analysed by48 and adult male huemul from the present study

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 331

body mass such as femur tibia humerus and radiusMeasurements on forelegs of three adult male huemul coincideclosely with correlations among 79 species analysed byChristiansen48 (Fig 2b)

Factors affecting body proportions

Constraints regarding body proportions are set by geneticshowever intraspecific variation is due to adaption followingecogeographical rules nutritional and physiologicallimitations4950 According to Flueck51 skeletal muscles areextremely plastic in their capacity to remodel according toalterations in physical demands such as in response to averageneeded muscle work as a function of terrain disturbances andfood density As most species fill the landscape along the fullspectrum of habitat qualities from source to sink areas bodyshapewill varywithin a species52 Scott53 observed that cervid leglong bones are highly variable depending on habitat usedpredator avoidance strategy used gait and locomotor patternemployed It is the distal limb segments (metapodials)however which undergo more length modification thanproximal segments121354ndash56

A most relevant ecogeographical pattern known since 1877Allenrsquos rule is found between climate and morphology as athermoregulatory adaptation This principle explains changes inratios of body surface area to body mass in hot and cold climatesand predicts short and broad limb proportions for animals incolder climates For instance bighorn sheep in cold climate haveshorter legs than bighorns in warm deserts57 Besides ampleempirical cases adaptions were shown experimentally in pig

litter mates raised at 35 20 and 5C (Fig 3a)58 or rats raised at28 and 5C54 colder temperature resulted in increased hairdensity and stockiness and shorter proportional leg lengthFurthermore oxygen pressure has also been recognised toinfluence bone growth With higher altitude increasinghypoxia results in reduced growth of distal limb bones alreadyat the fetal stage and thus proportionally shorter legs5960

Certain nutritional factors play well known roles in shapingbody proportions Iodine deficiency affects bone growth bydecreasing muscle function and thereby affecting boneremodelling and by direct effects on bone growthmetabolism506162 including shortening of metapodials andjoint disease6364 cretinism in its worst form including insheep and deer65 Selenium deficiency has a synergistic effectand produces shorter bones and overt osteopathology like Kasin-Beck disease6667 Andean mountains are deficient in iodine andselenium and may relate to high incidences of suchosteopathology in huemul68ndash70 Similarly a high prevalence ofosteoarthritis has been noted in moose (A alces) which wascorrelated with shorter metatarsals from nutritional constraints71

Corroborating trace mineral deficiency in huemul is the punyantler developmentnoted inmany remainingpopulations70whenconsidering the clear relationship between such deficiencies andreduced antler growth in other wild Odocoilines72

Discussion

lsquoMountain deerrsquo remains as a misconception about huemulIt originated from early explorers stressing the resemblance toibex chamois mountain sheep and mountain goats Howeverearly on huemul were described as rare and endangered andmany observations came from remote Andean refuge areas Inaddition the peculiar aggressive behaviour of huemul thehorseshoe posture and the very long hair coat may give animpression of stockiness These early casual statements aboutbody shape were later reenforced by key paleontological worklinking huemul to the fossil lsquomountain deerrsquo Navahoceros9 Thiswas an unfortunate error since the fossil was later shown to bea nomen nudum and corresponding to ancestral O lucasi10

Kurten also stated that huemul differed from Navahoceros byhaving two and not three tines on the antlers yet huemul haveup to five points673 Strikingly all of Kurtenrsquos comparisons tohuemul were also done only as casual statements withoutsupporting data yet his Navahoceros continues to enterphylogenetic interpretations323374

Thepresentmorphometric analysis shows for thefirst time thathuemul appendicular morphology is completely different fromthat of ungulates considered true rock climbers Thus neither theproportional metapodial lengths nor tibia metatarsal ratio normeasures of bone stoutness have any resemblance to rockclimbers Although bighorn sheep or chamois are consideredat times as lsquoinhabitants of rocky areasrsquo15 this applies equally wellto red deer7576 and even to American bison (ie lsquomountainbuffalorsquo) which lsquoused precipices so steep that hunters could notfollow them and even for dogs it was doubtful if they could havefollowed unharmedrsquo77 In little time exotic red deer haveinvaded all habitat types used now and in the past byhuemul78 confirming that both species can equally occupyAndean habitat types In fact of all species considered in this

Table 3 Comparison of stoutness among huemul ibex and red deerratios of appendicular bone length to articular width at distal and

proximal ends

Ibex Huemul Red deer Comparative stoutnessMaximal Minimal

Lengthdistal articular widthFemur 481 385 347 Red deer IbexTibia 85 727 897 Huemul Red deerMetatarsal 43 543 683 Ibex Red deerHumerus 485 502 467 Red deer HuemulRadius 474 535 559 Ibex Red deerMetacarpal 364 465 625 Ibex Red deer

Lengthproximal articularwidthFemur 406 423 363 Red deer HuemulTibia 5 492 461 Red deer IbexMetatarsal 526 609 699 Ibex Red deerHumerus 367 365 334 Red deer IbexRadius 46 522 497 Ibex HuemulMetacarpal 405 491 607 Ibex Red deer

Table 4 Percentage difference between half the tibial and totalmetatarsal lengths as an indication of affinity to a true rock climber15

Mountain Ibex Chamois Bighorn Huemul Redgoat sheep Male Female deer

+155 +21 ndash235 ndash27 ndash276 ndash307 ndash56

332 Animal Production Science W T Flueck and J M Smith-Flueck

paper those with proportional metatarsal length of 07ndash085(Table 2) are all well known to successfully inhabit rockyareas Instructively bighorn sheep and all species with longerproportional metapodials including chamois huemul and muledeer (Table 2) are also found in flat open areas Bighorns arewell known to inhabit or have inhabited low flat deserts andgrasslands7980 and sheep in general can do without rocks orcliffs Similarly chamois as an lsquoalpinersquo species is an artefact ofpast human-induced displacements81 since remains have beenfound down to near sea level82ndash84 as well as in rolling forest-coveredhillswhich they currently repopulate rapidly (nowcalledlsquoforest chamoisrsquo)8586 Lastly even Alpine ibex is a misnomer

extermination was much easier and much earlier at low andmedium altitude resulting in a prejudice in earlier years byreintroducing them to high elevations because that was wherethe last remaining groups were known from87 Recognised onlyrecently these reintroductions have actually created anartificial model of an animal of high altitude living there in allseasons above the tree line87ndash89 In contrast paleozoological datanow indicate that ibex occupied many additional topographicpositions than they do today89 Although ibex may remain inareas with some cliffs many fossils have been found down tosea level sometimes as dominant prey species in archeologicalsites and altitude clearly was not a factor in ibex ecology88 At

110

100

90

80

70

60

50

40

2 4 6 8 10 12

Species

Met

atar

sus

fem

ur (

)

14 16 18

1 data point

Lower limit

Upper limit

(a)

(b)

Fig 3 (a) Body proportions of pig litter mates raised at 35 and 5C fed to the sameweights58 (b) Intraspecificvariation in proportional leg length among several ungulates Sources are listed in Table 5 The species aremountain goat (1) tahr (2) ibex (3) Odocoileus virginianus (4) Rangifer tarandus (5) Bighorn sheep (6)huemul (7) Ovis dalli (8) Navahoceros (9) Ovis ammon (10) chamois (11) red deer (12) Dama dama (13)Odocoileus hemionus (14)O lucasi (15)Capreolus capreolus (16) Antilocapra americana (17) andAntilopecervicapra (18)

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 333

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

accepted rock specialists (mountain goats ibex tahr) are clearlyfar different even from bighorn sheep Speedy Black antelope onthe other extreme are also separated distinctly by proportionallymuch longer metatarsals

Among ungulates the tibia femur and radius humerus ratiosare rather uniform and corroborate that differences in legproportions relate mainly to metapodials1346 (Fig 2a) Amongspecies compared here (Table 2) standardised tibias varied byonly 47 whereas the metatarsals varied by 196 Alsoproportions between segments of the hind leg are very similarto those of the front leg in the same individual Asmetapodials areimportant for gait dynamics Table 2 shows the tibia metatarsalratio among ungulates A larger ratio means that metapodials areshorter and the pattern largely coincides with proportionalmetatarsal length Again the group of lsquotrue rock climbersrsquo hasthe largest tibia metatarsal ratios

Stoutness refers to bone length in relation to thickness orarticular width with smaller ratios indicating stouter bonesStout bones are the physiological reaction to forces and wouldgo in parallel with larger muscle masses Table 3 presents theratios of appendicular bone length in relation to articularwidth Huemul are compared with ibex (lsquotrue rock climberrsquo)and red deer as originating from steppes47 Out of the 12possibilities (six leg bones middot two ends) huemul only once hadthe stoutest yet three times the least stout articulate endsRemarkably ibex were stoutest and red deer the least stoutfor all metapodial ends (Table 3) Additionally in true rockclimbers tibia are the longest bone and metatarsals range fromjust over to just under half of tibial length15 again placinghuemul far from true rock climbers (Table 4)

Finally bone circumference as a measure of bone strength ishighly correlated with body mass in bones primarily supporting

Table 2 Proportional length of appendicular bones from various ungulates using the femur for a standard length (arranged according tometatarsal length)

Mountaingoat

Ibex Tahr Bighornsheep

Huemul Navahoceros Chamois Ovisammon

Tuleelk

Muledeer

Odocoileuslucasi

Reddeer

Antilopecervicapra

Femur 1 1 1 1 1 1 1 1 1 1 1 1 1Tibia 109 116 111 118 114 107 126 118 119 115 110 114 123Metatarsus 048 057 057 070 073 079 079 079 080 082 084 085 101

Tibiametatarsus 227 204 195 169 156 114 159 149 119 140 131 134 122

n 3 26ndash32 6 2 11ndash16 9ndash52 7 15 1 1 1 2 4Sex Male Male Mixed Unknown Male Unknown Male Male Unknown Unknown Male Male Mixed

100

10 000

circumference humerus79 species

79 species

circumference radius

male huemul (n = 3)

male huemul (n = 3)

1000

1000

100

1010 100 1000

Body mass (kg)

Body mass (kg)

Dim

ensi

on (

mm

)D

imen

sion

(m

m)

Weight (kg)

cm

10 000

100

1010 1000100 10 000

90

80

70

60

50

40

30

20

10

020 40 60 80 100 120 140 160

Hindleg

tibfemur

(a)(b)

Fig 2 (a) Tibia femur ratios among ungulates mentioned in the text in relation to leg length and arranged according to bodyweights (46 huemul from presentstudy) (b) Bone circumference in relation to body mass in 79 different species analysed by48 and adult male huemul from the present study

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 331

body mass such as femur tibia humerus and radiusMeasurements on forelegs of three adult male huemul coincideclosely with correlations among 79 species analysed byChristiansen48 (Fig 2b)

Factors affecting body proportions

Constraints regarding body proportions are set by geneticshowever intraspecific variation is due to adaption followingecogeographical rules nutritional and physiologicallimitations4950 According to Flueck51 skeletal muscles areextremely plastic in their capacity to remodel according toalterations in physical demands such as in response to averageneeded muscle work as a function of terrain disturbances andfood density As most species fill the landscape along the fullspectrum of habitat qualities from source to sink areas bodyshapewill varywithin a species52 Scott53 observed that cervid leglong bones are highly variable depending on habitat usedpredator avoidance strategy used gait and locomotor patternemployed It is the distal limb segments (metapodials)however which undergo more length modification thanproximal segments121354ndash56

A most relevant ecogeographical pattern known since 1877Allenrsquos rule is found between climate and morphology as athermoregulatory adaptation This principle explains changes inratios of body surface area to body mass in hot and cold climatesand predicts short and broad limb proportions for animals incolder climates For instance bighorn sheep in cold climate haveshorter legs than bighorns in warm deserts57 Besides ampleempirical cases adaptions were shown experimentally in pig

litter mates raised at 35 20 and 5C (Fig 3a)58 or rats raised at28 and 5C54 colder temperature resulted in increased hairdensity and stockiness and shorter proportional leg lengthFurthermore oxygen pressure has also been recognised toinfluence bone growth With higher altitude increasinghypoxia results in reduced growth of distal limb bones alreadyat the fetal stage and thus proportionally shorter legs5960

Certain nutritional factors play well known roles in shapingbody proportions Iodine deficiency affects bone growth bydecreasing muscle function and thereby affecting boneremodelling and by direct effects on bone growthmetabolism506162 including shortening of metapodials andjoint disease6364 cretinism in its worst form including insheep and deer65 Selenium deficiency has a synergistic effectand produces shorter bones and overt osteopathology like Kasin-Beck disease6667 Andean mountains are deficient in iodine andselenium and may relate to high incidences of suchosteopathology in huemul68ndash70 Similarly a high prevalence ofosteoarthritis has been noted in moose (A alces) which wascorrelated with shorter metatarsals from nutritional constraints71

Corroborating trace mineral deficiency in huemul is the punyantler developmentnoted inmany remainingpopulations70whenconsidering the clear relationship between such deficiencies andreduced antler growth in other wild Odocoilines72

Discussion

lsquoMountain deerrsquo remains as a misconception about huemulIt originated from early explorers stressing the resemblance toibex chamois mountain sheep and mountain goats Howeverearly on huemul were described as rare and endangered andmany observations came from remote Andean refuge areas Inaddition the peculiar aggressive behaviour of huemul thehorseshoe posture and the very long hair coat may give animpression of stockiness These early casual statements aboutbody shape were later reenforced by key paleontological worklinking huemul to the fossil lsquomountain deerrsquo Navahoceros9 Thiswas an unfortunate error since the fossil was later shown to bea nomen nudum and corresponding to ancestral O lucasi10

Kurten also stated that huemul differed from Navahoceros byhaving two and not three tines on the antlers yet huemul haveup to five points673 Strikingly all of Kurtenrsquos comparisons tohuemul were also done only as casual statements withoutsupporting data yet his Navahoceros continues to enterphylogenetic interpretations323374

Thepresentmorphometric analysis shows for thefirst time thathuemul appendicular morphology is completely different fromthat of ungulates considered true rock climbers Thus neither theproportional metapodial lengths nor tibia metatarsal ratio normeasures of bone stoutness have any resemblance to rockclimbers Although bighorn sheep or chamois are consideredat times as lsquoinhabitants of rocky areasrsquo15 this applies equally wellto red deer7576 and even to American bison (ie lsquomountainbuffalorsquo) which lsquoused precipices so steep that hunters could notfollow them and even for dogs it was doubtful if they could havefollowed unharmedrsquo77 In little time exotic red deer haveinvaded all habitat types used now and in the past byhuemul78 confirming that both species can equally occupyAndean habitat types In fact of all species considered in this

Table 3 Comparison of stoutness among huemul ibex and red deerratios of appendicular bone length to articular width at distal and

proximal ends

Ibex Huemul Red deer Comparative stoutnessMaximal Minimal

Lengthdistal articular widthFemur 481 385 347 Red deer IbexTibia 85 727 897 Huemul Red deerMetatarsal 43 543 683 Ibex Red deerHumerus 485 502 467 Red deer HuemulRadius 474 535 559 Ibex Red deerMetacarpal 364 465 625 Ibex Red deer

Lengthproximal articularwidthFemur 406 423 363 Red deer HuemulTibia 5 492 461 Red deer IbexMetatarsal 526 609 699 Ibex Red deerHumerus 367 365 334 Red deer IbexRadius 46 522 497 Ibex HuemulMetacarpal 405 491 607 Ibex Red deer

Table 4 Percentage difference between half the tibial and totalmetatarsal lengths as an indication of affinity to a true rock climber15

Mountain Ibex Chamois Bighorn Huemul Redgoat sheep Male Female deer

+155 +21 ndash235 ndash27 ndash276 ndash307 ndash56

332 Animal Production Science W T Flueck and J M Smith-Flueck

paper those with proportional metatarsal length of 07ndash085(Table 2) are all well known to successfully inhabit rockyareas Instructively bighorn sheep and all species with longerproportional metapodials including chamois huemul and muledeer (Table 2) are also found in flat open areas Bighorns arewell known to inhabit or have inhabited low flat deserts andgrasslands7980 and sheep in general can do without rocks orcliffs Similarly chamois as an lsquoalpinersquo species is an artefact ofpast human-induced displacements81 since remains have beenfound down to near sea level82ndash84 as well as in rolling forest-coveredhillswhich they currently repopulate rapidly (nowcalledlsquoforest chamoisrsquo)8586 Lastly even Alpine ibex is a misnomer

extermination was much easier and much earlier at low andmedium altitude resulting in a prejudice in earlier years byreintroducing them to high elevations because that was wherethe last remaining groups were known from87 Recognised onlyrecently these reintroductions have actually created anartificial model of an animal of high altitude living there in allseasons above the tree line87ndash89 In contrast paleozoological datanow indicate that ibex occupied many additional topographicpositions than they do today89 Although ibex may remain inareas with some cliffs many fossils have been found down tosea level sometimes as dominant prey species in archeologicalsites and altitude clearly was not a factor in ibex ecology88 At

110

100

90

80

70

60

50

40

2 4 6 8 10 12

Species

Met

atar

sus

fem

ur (

)

14 16 18

1 data point

Lower limit

Upper limit

(a)

(b)

Fig 3 (a) Body proportions of pig litter mates raised at 35 and 5C fed to the sameweights58 (b) Intraspecificvariation in proportional leg length among several ungulates Sources are listed in Table 5 The species aremountain goat (1) tahr (2) ibex (3) Odocoileus virginianus (4) Rangifer tarandus (5) Bighorn sheep (6)huemul (7) Ovis dalli (8) Navahoceros (9) Ovis ammon (10) chamois (11) red deer (12) Dama dama (13)Odocoileus hemionus (14)O lucasi (15)Capreolus capreolus (16) Antilocapra americana (17) andAntilopecervicapra (18)

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 333

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

body mass such as femur tibia humerus and radiusMeasurements on forelegs of three adult male huemul coincideclosely with correlations among 79 species analysed byChristiansen48 (Fig 2b)

Factors affecting body proportions

Constraints regarding body proportions are set by geneticshowever intraspecific variation is due to adaption followingecogeographical rules nutritional and physiologicallimitations4950 According to Flueck51 skeletal muscles areextremely plastic in their capacity to remodel according toalterations in physical demands such as in response to averageneeded muscle work as a function of terrain disturbances andfood density As most species fill the landscape along the fullspectrum of habitat qualities from source to sink areas bodyshapewill varywithin a species52 Scott53 observed that cervid leglong bones are highly variable depending on habitat usedpredator avoidance strategy used gait and locomotor patternemployed It is the distal limb segments (metapodials)however which undergo more length modification thanproximal segments121354ndash56

A most relevant ecogeographical pattern known since 1877Allenrsquos rule is found between climate and morphology as athermoregulatory adaptation This principle explains changes inratios of body surface area to body mass in hot and cold climatesand predicts short and broad limb proportions for animals incolder climates For instance bighorn sheep in cold climate haveshorter legs than bighorns in warm deserts57 Besides ampleempirical cases adaptions were shown experimentally in pig

litter mates raised at 35 20 and 5C (Fig 3a)58 or rats raised at28 and 5C54 colder temperature resulted in increased hairdensity and stockiness and shorter proportional leg lengthFurthermore oxygen pressure has also been recognised toinfluence bone growth With higher altitude increasinghypoxia results in reduced growth of distal limb bones alreadyat the fetal stage and thus proportionally shorter legs5960

Certain nutritional factors play well known roles in shapingbody proportions Iodine deficiency affects bone growth bydecreasing muscle function and thereby affecting boneremodelling and by direct effects on bone growthmetabolism506162 including shortening of metapodials andjoint disease6364 cretinism in its worst form including insheep and deer65 Selenium deficiency has a synergistic effectand produces shorter bones and overt osteopathology like Kasin-Beck disease6667 Andean mountains are deficient in iodine andselenium and may relate to high incidences of suchosteopathology in huemul68ndash70 Similarly a high prevalence ofosteoarthritis has been noted in moose (A alces) which wascorrelated with shorter metatarsals from nutritional constraints71

Corroborating trace mineral deficiency in huemul is the punyantler developmentnoted inmany remainingpopulations70whenconsidering the clear relationship between such deficiencies andreduced antler growth in other wild Odocoilines72

Discussion

lsquoMountain deerrsquo remains as a misconception about huemulIt originated from early explorers stressing the resemblance toibex chamois mountain sheep and mountain goats Howeverearly on huemul were described as rare and endangered andmany observations came from remote Andean refuge areas Inaddition the peculiar aggressive behaviour of huemul thehorseshoe posture and the very long hair coat may give animpression of stockiness These early casual statements aboutbody shape were later reenforced by key paleontological worklinking huemul to the fossil lsquomountain deerrsquo Navahoceros9 Thiswas an unfortunate error since the fossil was later shown to bea nomen nudum and corresponding to ancestral O lucasi10

Kurten also stated that huemul differed from Navahoceros byhaving two and not three tines on the antlers yet huemul haveup to five points673 Strikingly all of Kurtenrsquos comparisons tohuemul were also done only as casual statements withoutsupporting data yet his Navahoceros continues to enterphylogenetic interpretations323374

Thepresentmorphometric analysis shows for thefirst time thathuemul appendicular morphology is completely different fromthat of ungulates considered true rock climbers Thus neither theproportional metapodial lengths nor tibia metatarsal ratio normeasures of bone stoutness have any resemblance to rockclimbers Although bighorn sheep or chamois are consideredat times as lsquoinhabitants of rocky areasrsquo15 this applies equally wellto red deer7576 and even to American bison (ie lsquomountainbuffalorsquo) which lsquoused precipices so steep that hunters could notfollow them and even for dogs it was doubtful if they could havefollowed unharmedrsquo77 In little time exotic red deer haveinvaded all habitat types used now and in the past byhuemul78 confirming that both species can equally occupyAndean habitat types In fact of all species considered in this

Table 3 Comparison of stoutness among huemul ibex and red deerratios of appendicular bone length to articular width at distal and

proximal ends

Ibex Huemul Red deer Comparative stoutnessMaximal Minimal

Lengthdistal articular widthFemur 481 385 347 Red deer IbexTibia 85 727 897 Huemul Red deerMetatarsal 43 543 683 Ibex Red deerHumerus 485 502 467 Red deer HuemulRadius 474 535 559 Ibex Red deerMetacarpal 364 465 625 Ibex Red deer

Lengthproximal articularwidthFemur 406 423 363 Red deer HuemulTibia 5 492 461 Red deer IbexMetatarsal 526 609 699 Ibex Red deerHumerus 367 365 334 Red deer IbexRadius 46 522 497 Ibex HuemulMetacarpal 405 491 607 Ibex Red deer

Table 4 Percentage difference between half the tibial and totalmetatarsal lengths as an indication of affinity to a true rock climber15

Mountain Ibex Chamois Bighorn Huemul Redgoat sheep Male Female deer

+155 +21 ndash235 ndash27 ndash276 ndash307 ndash56

332 Animal Production Science W T Flueck and J M Smith-Flueck

paper those with proportional metatarsal length of 07ndash085(Table 2) are all well known to successfully inhabit rockyareas Instructively bighorn sheep and all species with longerproportional metapodials including chamois huemul and muledeer (Table 2) are also found in flat open areas Bighorns arewell known to inhabit or have inhabited low flat deserts andgrasslands7980 and sheep in general can do without rocks orcliffs Similarly chamois as an lsquoalpinersquo species is an artefact ofpast human-induced displacements81 since remains have beenfound down to near sea level82ndash84 as well as in rolling forest-coveredhillswhich they currently repopulate rapidly (nowcalledlsquoforest chamoisrsquo)8586 Lastly even Alpine ibex is a misnomer

extermination was much easier and much earlier at low andmedium altitude resulting in a prejudice in earlier years byreintroducing them to high elevations because that was wherethe last remaining groups were known from87 Recognised onlyrecently these reintroductions have actually created anartificial model of an animal of high altitude living there in allseasons above the tree line87ndash89 In contrast paleozoological datanow indicate that ibex occupied many additional topographicpositions than they do today89 Although ibex may remain inareas with some cliffs many fossils have been found down tosea level sometimes as dominant prey species in archeologicalsites and altitude clearly was not a factor in ibex ecology88 At

110

100

90

80

70

60

50

40

2 4 6 8 10 12

Species

Met

atar

sus

fem

ur (

)

14 16 18

1 data point

Lower limit

Upper limit

(a)

(b)

Fig 3 (a) Body proportions of pig litter mates raised at 35 and 5C fed to the sameweights58 (b) Intraspecificvariation in proportional leg length among several ungulates Sources are listed in Table 5 The species aremountain goat (1) tahr (2) ibex (3) Odocoileus virginianus (4) Rangifer tarandus (5) Bighorn sheep (6)huemul (7) Ovis dalli (8) Navahoceros (9) Ovis ammon (10) chamois (11) red deer (12) Dama dama (13)Odocoileus hemionus (14)O lucasi (15)Capreolus capreolus (16) Antilocapra americana (17) andAntilopecervicapra (18)

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 333

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

paper those with proportional metatarsal length of 07ndash085(Table 2) are all well known to successfully inhabit rockyareas Instructively bighorn sheep and all species with longerproportional metapodials including chamois huemul and muledeer (Table 2) are also found in flat open areas Bighorns arewell known to inhabit or have inhabited low flat deserts andgrasslands7980 and sheep in general can do without rocks orcliffs Similarly chamois as an lsquoalpinersquo species is an artefact ofpast human-induced displacements81 since remains have beenfound down to near sea level82ndash84 as well as in rolling forest-coveredhillswhich they currently repopulate rapidly (nowcalledlsquoforest chamoisrsquo)8586 Lastly even Alpine ibex is a misnomer

extermination was much easier and much earlier at low andmedium altitude resulting in a prejudice in earlier years byreintroducing them to high elevations because that was wherethe last remaining groups were known from87 Recognised onlyrecently these reintroductions have actually created anartificial model of an animal of high altitude living there in allseasons above the tree line87ndash89 In contrast paleozoological datanow indicate that ibex occupied many additional topographicpositions than they do today89 Although ibex may remain inareas with some cliffs many fossils have been found down tosea level sometimes as dominant prey species in archeologicalsites and altitude clearly was not a factor in ibex ecology88 At

110

100

90

80

70

60

50

40

2 4 6 8 10 12

Species

Met

atar

sus

fem

ur (

)

14 16 18

1 data point

Lower limit

Upper limit

(a)

(b)

Fig 3 (a) Body proportions of pig litter mates raised at 35 and 5C fed to the sameweights58 (b) Intraspecificvariation in proportional leg length among several ungulates Sources are listed in Table 5 The species aremountain goat (1) tahr (2) ibex (3) Odocoileus virginianus (4) Rangifer tarandus (5) Bighorn sheep (6)huemul (7) Ovis dalli (8) Navahoceros (9) Ovis ammon (10) chamois (11) red deer (12) Dama dama (13)Odocoileus hemionus (14)O lucasi (15)Capreolus capreolus (16) Antilocapra americana (17) andAntilopecervicapra (18)

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 333

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

low elevation sites ibex were associated with all the othermain ungulate species also exploited by humans Recentreintroductions to very low elevation areas were thussuccessful and there are cases of natural recolonisation fromhigh elevation populations to low elevation areas90 Thereforehistoric comparisons of huemul to ibex and chamois were doneunder the misbelief that both latter species are specialists forhigh altitudes and extreme rocky areas the only link betweenthese three species however appears to be historic anthropicdisplacement from favourable habitats Observations by Scott53

coincide in that no cervids are occupying the type of cliffhabitat as do Caprini and at times Rupicapra Moreover it isno surprise that the only sister species to huemul Hippocamelusantisensis is considered osteologically indistinguishable andeven considered a mere subspecies162591 yet besides usingsome forest types92 its current habitat is mainly treelessgrasslands with high affinity to Patagonian grasslandscoexisting with several camelid species

The literature is replete with empirical and experimental datashowing intraspecific variation in proportional bone growth andseveral causative factors are well known As the metapodialsundergo major length modifications compared with the proximalleg bone segments we would expect to find large intraspecificvariation in proportional leg length which in turn has beensubstantiated (Table 5) For instance relative leg length isconsiderably greater in forest reindeer than in mountain

reindeer93 and shoulder height is reported to differ by 15 cmbetween forest- and alpine-wintering groups without differencesin other body measurements or proportions9495 Importantlychanges in leg proportions inRangifer have been observedwithinone single population after only 30ndash35 years of nutritionalstress (96 also see49) Odocoileus virginianus from twodifferent environments had proportionally different hindfoot lengths such that populations could be distinguished withr = 092 at P lt 0000197 similar to studies on mule deer98 andCapreolus capreolus99 The currently small sample size ofhuemul and mainly from one reduced population shows onlysmall variations however other better studied ruminants give anindication of possible variability of proportional leg length(Fig 3b) Importantly some populations of Rangifer and evenO virginianus have much shorter legs than our huemul samplewith metatarsals proportionally 14 shorter than huemul(Table 5)

Skeletal proportions are affected by numerous factors Somemorphological differences of proportional limb bone lengthsresult from adaption to different environmental regimes ratherthan reflecting phylogeny101356 Van derMeuleun and Carter100

concluded that long bone scaling is not a result of intrinsicgenetic factors but is the result of highly conserved extrinsicbiophysical processes whereby bone tissue strains modulateskeletal morphogenesis This is due to epigenetic componentsof skeletal design that is continuously updated in response to the

Table 5 Variation of proportional metatarsal or hind foot length (HL) among various cervid species and somecomparative ratios from other ungulates

Species Sex Femurmetatarsus difference Reference

CervidsRangifer tarandus Male 100 89ndash100 108 21 96

R tarandus Female 100 93ndash100 109 17 96

R tarandus Unknown 100 64ndash100 99 55 12

R tarandus Mixed 100 64ndash100 109 70 1296

Odocoileus virginianus Unknown 100 63ndash100 90 43 12

O hemionusA Unknown 100 86ndash100 100 16 91146

O hemionus Unknown 100 82 22 1112

O lucasi Unknown 100 84 10

Dama dama Unknown 100 82ndash100 92 12 1246

Cervus elaphus Unknown 100 80ndash100 96 20 1246

Capreolus capreolus Unknown 100 86ndash100 100 16 1246

Hippocamelus bisulcus Male 100 72ndash100 75 4 n = 8 this studyH bisulcus Female 100 73ndash100 76 4 n = 3 this study

Other ungulatesOreamnos americanus Unknown 100 46ndash100 55 20 121346

Capra ibex Mixed 100 57ndash100 60 5 14

Ovis ammon Unknown 100 79ndash100 83 5 1346106

Rupicapra rupicapra Unknown 100 77ndash100 82 7 1246

O canadensis Unknown 100 70ndash100 75 7 1213

O dalli Unknown 100 72 ndash 12

Antilocapra americana Unknown 100 96 ndash46

Antilope cervicapra Unknown 100 101 ndash13

Species Sex Body lengthHL difference Reference

Rangifer tarandus Male 100 20ndash100 62 310 96

Female 100 26ndash100 34 31 96

AData as HL in reference11 was adjusted by halving to approximate metatarsal length

334 Animal Production Science W T Flueck and J M Smith-Flueck

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

mechanical forces exerted on the bones51101 Muscle force is thesingle most important factor in determining the amount of forcethe bonesmust resist as these forces surpass several fold the stressimposed from static weight48101ndash103 Major forces result fromlocomotion and the change in limb posture accounts for most ofthe reduction in bone stress among small to rather largemammals48101 Only a short duration of mechanical loading isnecessary to initiate an adaptive bone response and extending theloading duration has a diminishing effect on further boneadaptation101 Furthermore long bones lose considerable bonemass when they are not mechanically loaded Lastly strongeffects on proportional leg length result from nutritionalconstraints which in central Andean habitats of huemul arenotably deficiencies of phosphorous iodine and seleniumThese and other analyses clearly show the extraordinarydegree to which the skeleton can adapt to differences inmechanical loading as induced from different habitat typesand locomotor needs and to nutritional constraints51100104

The nutritional ecology of remnant huemul populations70 andthe climatic and topographic features of localities wherehuemul currently remain indicate that leg proportions ofhuemul from these sites would be expected to be at the lowend of the potential range of variations for the species inresponse to local adaption In contrast populations which inthe past existed in more open rolling landscapes would beexpected to have had individuals with notably longerproportional leg lengths Nonetheless extant huemulparticularly if not in an alert stance and in summer coat oftencan hardly be qualified as being short-legged (Fig 4)

Conclusion

Huemul had a much wider distribution in pre-Spanish timesthan in more recent times of explorations and settlement

of Patagonia Accordingly a few historic accounts stilldocumented presence in the eastern treeless lowlandsindicating that huemul was well suited to exploit those areas(Fig 5)7 We caution against the rigid application of modernhuemul habitat use in interpreting past habitat use and simplyignoring the few historic extra-Andean accounts as abnormaloutliers Clear evidence7 even if rare of past presence has to beaccepted and should not be dismissed as shown for chamois andibex Indeed huemul ecology must be interpreted in terms offirst principles rather than applying direct analogues from thepresent This allows us to begin to use the past to understand thepresent instead of repeating the fallacy of imposing the presenton the past

Current efforts to recover remaining huemul are distinctlybased on the assumption that huemul foremost belong in ruggedmountains because of their supposed special adaptions andresemblance to stereotype ungulates erroneously believed toonly occur in rugged mountains elsewhere However such asupposed specialisation is not reflected by the evolutionaryhistory of huemul and current ecological realities wererecently created from human impacts These claims alsounderscore the continuous ignoring of historic accounts ofhuemul in steppes far from the Andean forests condemned tobe at most a footnote Anecdotal and inconclusive physical dataare often used to assess the current ranges of rare or elusivespecies However the use of such data for species conservationcan lead to large errors of omission and commission which caninfluence the efficacy of subsequent conservation efforts105 Thepresent empirical comparisons show huemul leg morphology tofall well within that of other cervids and can be expected to varysubstantially if they were to live in habitats formerly used Itsupports many other lines of evidence that huemul existed intreeless habitat and colonisedAndean forests and higher altitudes

Fig 4 Body shapes of several extant huemul that are not in an alert stance and with summer coat

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 335

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

(a) (b) (c)

(d ) (e )

(f )

Fig 5 Huemul habitat far from forests and in flat or rolling landscapes (a) Landscape by Port Desire at Atlantic coast (47440S 65540W)where several reports mentioned huemul7 (b) Huemul in steppe approached by gaucho from Onelli 1904 (c) Huemul photographed in the1920sbyAGrosse (d e) Princetonexpeditions late 1800s huntinghuemul as far as 200kmfrom forests ( f ) Extant huemul periglacial Pacificcoast old moraines flat wide valley bottoms

336 Animal Production Science W T Flueck and J M Smith-Flueck

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

secondarily and habitat breadth of huemul is thus more like thatfound in other closely related Odocoilines This promisestremendous new opportunities for recovery efforts byconsidering reintroductions to other portions of the landscapeused formerly by huemul which tend to be more productive sitesthan those currently occupied by many huemul groups

Acknowledgements

We thank Loic Costeur for access to collections of ungulate skeletons atthe Naturhistorisches Museum Basel-Switzerland Oscar Guineo for theChilean data and Charles Dailey Bruce Mincher and two anonymousreviewers for their constructive criticism of this paper World NatureAssociation Wildlife Conservation International Scott Neotropical FundNorton Bodega Argentina New Zealandrsquos Swazi Ltd and the ZoologischeGesellschaft fuumlr Arten- und Populationsschutz financially supported ourfield work and numerous volunteers from many countries assisted withfield work over the years thanks to all of them

References

1 Eisenberg JF The evolutionary history of the Cervidae with specialreference to the South American radiation In Wemmer CM editorBiology and management of the Cervidae Washington DCSmithsonian Institution Press 1987 pp 60ndash64

2 IriarteAMamiferos deChile Barcelona Spain LynxEdiciones 20083 Gueacuterin C Faure M The Cervidae (Mammalia Artiodactyla) of the

Upper PleistoceneLower Holocene deposits of the Serra da CapivaraNational Park Region (Piaui Brazil) Geobios 2009 42 169ndash95

4 Muntildeoz-Pedreros A Valenzuela JY Mamiferos de Chile Segundaedicion Valdivia Chile CEA Ediciones 2009

5 Vila AR Saucedo C Aldridge D Ramilo E Corti P South Andeanhuemul Hippocamelus bisulcus (Molina 1782) In Barbanti MGonzaacutelez S editors Neotropical Cervidology Brazil FUNEP 2010pp 89ndash100

6 OsgoodWHThemammals of ChileFieldMuseumof NaturalHistoryZoological Series 1943 30 1ndash268

7 Diacuteaz NI Changes in the range distribution ofHippocamelus bisulcus inPatagonia Z Saugetierkd 1993 58 344ndash51

8 Flueck WT Smith-Flueck JM Predicaments of endangered huemuldeer Hippocamelus bisulcus in Argentina a review Eur J Wildl Res2006 52 69ndash80 doi101007s10344-005-0020-4

9 Kurten B A new pleistocene genus of American mountain deerJ Mammal 1975 56 507ndash8 doi1023071379377

10 Morejohn GV Dailey DC The identity and postcranial osteology ofOdocoileus lucasi (Hay) 1927 Sierra College Natural HistoryMuseumBulletin 2004 1 1ndash54

11 Klein DR Range-related differences in growth of deer reflected inskeletal ratios J Mammal 1964 45 226ndash35 doi1023071376985

12 McMahon TA Allometry and biomechanics limbbones in adultungulates Am Nat 1975 109 547ndash63 doi101086283026

13 Scott KM Allometric trends and locomotor adaptations in the BovidaeBull Am Mus Nat Hist 1985 179 197ndash288

14 Fernandez H Monchot H Sexual dimorphism in limb bones of Ibex(Capra ibex L) mixture analysis applied to modern and fossil dataInt J Osteoarchaeol 2007 17 479ndash91 doi101002oa876

15 Whistler DP Webb SD New goatlike camelid from the late Plioceneof Tecopa lake basin California Contrib Sci 2005 503 1ndash40

16 Philippi RA Uumlber denGuemul vonMolinaArchiv fuumlr Naturgeschichte1857 23 135ndash6

17 Gigoux EE El huemul Rev Chil Hist Nat 1929 23 573ndash8218 Wolffsohn JW Notas sobre el huemul Rev Chil Hist Nat 1910 14

227ndash3419 Latcham RE Expedicion cientifica Macqueen al Aysen Boletin del

Museo Nacional (Chile) 1935 14 7ndash31

20 De Agostini AM Andes Patagoacutenicos Viajes de Exploracioacuten a laCordillera Patagoacutenica Austral Buenos Aires Talleres GraacuteficosGuillermo Kraft Ltda 1941

21 Ringuelet RA Serie Teacutecnica y Didaacutectica Nr 2 Temas de CienciaNaturales La Plata Argentina ProBiotA 2003 Divisioacuten ZoologiacuteaVertebrados Museo de La Plata 1946

22 Grosse A El huemul ndash ciervo de los Andes y emblema del escudoChileno [Revista Chileno Alemana] Condor 1949 12 10ndash12

23 Pefaacuteur J Hermosilla W DiCastri F Gonzaacutelez R Salinas F Estudiopreliminar de mamiacuteferos silvestres chilenos su distribucioacuten valoreconoacutemico e importancia zoonoacutetica Revista de la SociedadMedicina Veterinaria (Chile) 1968 18 3ndash15

24 Franke FR Mein Inselparadies Bern Switzerland Verlag A FranckeAG 1949

25 Krieg H Biologische Reisestudien in Suumldamerika V Die chilenischenHirsche Z Morphol Oekol Tiere 1925 4 585ndash97 doi101007BF00407652

26 Kolliker Frers A Das Waidwerk und die autochthonen Cerviden inArgentinien In Vogel CA editor Parque Diana Muumlnchen GermanyStefan Schwarz Verlag 1969 pp 25ndash31

27 Fraumldrich H Bemerkungen uumlber Nord-Andenhirsche (Hippocamelusantisensis) im Berliner Zoo Bongo Berlin 1978 2 81ndash8

28 Kurten B A stilt-legged deer Sangamona of the North-AmericanPleistocene Boreas 1979 8 313ndash21 doi101111j1502-38851979tb00815x

29 Povilitis A The Chilean Huemul Project ndash a case history (1975ndash1976)In Threatened Deer Gland Switzerland IUCN 1978 pp 109ndash128

30 Povilitis A The huemul in Chile national symbol in jeopardy Oryx1983 17 34ndash40 doi101017S003060530001838X

31 Delegacion Regional Patagonia Programa conservacioacuten del huemul dela Administracioacuten de Parques Nacionales en Argentina (15 antildeos1993ndash2007) Informe 2007 1ndash19

32 WebbSDA craniumofNavahoceros and its phylogenetic place amongNew World Cervidae Ann Zool Fenn 1992 28 401ndash10

33 Webb SD Evolutionary history of New World Cervidae In Vrba ESSchaller GB editors Antelopes deer and relatives New York YaleUniversity Press 2000 pp 38ndash64

34 BarnoskyADHadlyEAMaurerBAChristieMITemperate terrestrialvertebrate faunas in North and South America interplay of ecologyevolution and geography with biodiversity Conserv Biol 2001 15658ndash674 doi101046j1523-17392001015003658x

35 Churcher CS Sangamona the furtive deer In Genoways HH DawsenMR editors Contributions in quarternary vertebrate paleonotology avolume in memorial to John D Guilday Carnegie Museum of NaturalHistory Special Publication 1984 8 316ndash31

36 Wheatley PV Ruez DR Pliocene Odocoileus from Hagerman FossilBeds National Monument Idaho and comments on the taxonomicstatus of Odocoileus brachyodontus J Vertebr Paleontol 2006 26462ndash5 doi1016710272-4634(2006)26[462POFHFB]20CO2

37 Smith-Flueck JM The current situation of the Patagonian huemul InDiacuteaz NI Smith-Flueck JM editors The Patagonian huemul amysterious deer on the brink of extinction Buenos Aires LOLA2000 pp 67ndash146

38 Brandborg SM Life history and management of the mountain goat inIdahoWildlife Bulletin Department of Fish and Game State of IdahoBoise Idaho 1955 2 1ndash142

39 Honess RF Frost NM A Wyoming bighorn sheep study WyomingGame and Fish Department Bulletin 1942 1 1ndash127

40 Cowan IMcT Geist V Aggressive behavior in deer of the genusOdocoileus J Mammal 1961 42 522ndash6 doi1023071377372

41 Bubenik AB Significance of antlers in the social life of barren groundcaribou Biological Papers University of Alaska Special Report 19751 436ndash61

42 Crichton V The horseshoe posture in moose ndash a reaction to perceivedthreats Alces 2002 38 109ndash11

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 337

43 TexeraWAAlgunos aspectos de la biologiacutea del huemul (Hippocamelusbisulcus) (MammaliaArtiodactyla Cervidae) en cautividadAnales delInstituo de la Patagonia Punta Arenas (Chile) 1974 5 155ndash88

44 Guineo P Guineo Garay R Garay G Conociendo al huemul de Torresdel Paine Punta Arenas Chile La Prensa Austral 2008

45 Garland T Janis CM Does metatarsal femur ratio predict maximalrunning speed in cursorial mammals J Zool 1993 229 133ndash51doi101111j1469-79981993tb02626x

46 Christiansen P Locomotion in terrestrial mammals the influence ofbody mass limb length and bone proportions on speed Zool J Linn Soc2002 136 685ndash714 doi101046j1096-3642200200041x

47 GeistVDeer of theworld PennsylvaniaUSAStackpoleBooks 199848 ChristiansenP Scaling of the limb long bones to bodymass in terrestrial

mammals J Morphol 1999 239 167ndash90 doi101002(SICI)1097-4687(199902)2392lt167AID-JMOR5gt30CO2-8

49 Palsson H Verges JB Effects of the plane of nutrition on growth anddevelopment of carcass quality in lambs Part I The effects of high andlow planes of nutrition at different ages J Agric Sci 1952 42 1ndash92doi101017S0021859600058718

50 Nilsson O Baron J Fundamental limits on longitudinal bone growthgrowth plate senescence and epiphyseal fusion Trends EndocrinolMetab 2004 15 370ndash4

51 FlueckM Functional structural andmolecular plasticity ofmammalianskeletal muscle in response to exercise stimuli J Exp Biol 2006 2092239ndash48 doi101242jeb02149

52 Putman R Flueck WT Intraspecific variation in biology and ecologyof deer magnitude and causation 2011 51 277ndash91 doi101071AN10169

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55 Holliday TWRuff CB Relative variation in human proximal and distallimb segment lengths Am J Phys Anthropol 2001 116 26ndash33doi101002ajpa1098

56 Lilje KE Tardieu C Fischer MS Scaling of long bones in ruminantswith respect to the scapula JZoological Syst EvolRes2003 41 118ndash26doi101046j1439-0469200300207x

57 McCutchen HE Desert bighorn zoogeography and adaptation inrelation to historic land use Wildl Soc Bull 1981 9 171ndash9

58 Weaver M IngramDMorphological changes in swine associated withenvironmental temperature Ecology 1969 50 710ndash3 doi1023071936264

59 Weinstein KJ Body proportions in ancient Andeans from high andlow altitudes Am J Phys Anthropol 2005 128 569ndash85 doi101002ajpa20137

60 Bailey SM Xu J Feng JH Hu X Zhang C Qui S Tradeoffs betweenoxygenand energy in tibial growth at high altitudeAmJHumBiol200719 662ndash8 doi101002ajhb20667

61 Harrison AP Tivey DR Clausen T Duchamp C DaunceyMJ Role ofthyroid hormones in early postnatal development of skeletal muscle andits implications for undernutition Br J Nutr 1996 76 841ndash55doi101079BJN19960091

62 Oestreich AE The acrophysis a unifying concept for understandingenchondral bonegrowth and its disorders IIAbnormal growthSkeletalRadiol 2004 33 119ndash28 doi101007s00256-003-0735-9

63 McLean RM Podell DN Bone and joint manifestations ofhypothyroidism Semin Arthritis Rheum 1995 24 282ndash90doi101016S0049-0172(95)80038-7

64 Obendorf PJ Oxnard CE Kefford BJ Are the small human-like fossilsfound on Flores human endemic cretins Proc Biol Sci 2008 2751287ndash96 doi101098rspb20071488

65 Crile R The comparative anatomy of the thyroid and adrenal glandsin wild animals Ohio J Sci 1937 37 42ndash61

66 Moreno-Reyes R Suetens CMathieu F Begaux F Zhu D RiveraMTBoelaert M Negraveve J Perlmutter N Vanderpas J Kashin-Beckosteoarthropathy in rural Tibet in relation to selenium and iodinestatus N Engl J Med 1998 339 1112ndash20 doi101056NEJM199810153391604

67 Ren FL Guo X Zhang RJ Wang SJ Zuo H Zhang ZT Geng DYu Y Su M Effects of selenium and iodine deficiency on bonecartilage growth plate and chondrocyte differentiation in twogenerations of rats Osteoarthritis Cartilage 2007 15 1171ndash7doi101016jjoca200703013

68 Flueck WT Smith-Flueck JM Why the Patagonian huemul deer inArgentina fails to recover an ecological hypothesis In Bartos LDusek A Kotrba R Bartosova J editors Advances in deer biologydeer in a changing world Praha Czech Republic Research Institute ofAnimal Production 2006 pp 181ndash185

69 Flueck WT Smith-Flueck JM Age-independent osteopathology inskeletons of a South American cervid the Patagonian huemul(Hippocamelus bisulcus) J Wildl Dis 2008 44 636ndash48

70 Flueck WT Smith-Flueck JM Recent advances in the nutritionalecology of the Patagonian huemul implications for recovery AnimProd Sci 2011 51 311ndash26 doi101071AN10237

71 Peterson RO Vucetich JA Fenton G Drummer TD Larsen CSEcology of arthritis Ecol Lett 2010 13 1124ndash8 doi101111j1461-0248201001504x

72 Lehoczki R Erdeacutelyi K Sonkoly K Szemethy L Csaacutenyi S Iodinedistribution in the environment as a limiting factor for roe deer antlerdevelopment Biol Trace Elem Res 2010 139 168ndash76 doi101007s12011-010-8655-8

73 Rusconi C Anomalias en las cornamentas del huemulAnales SociedadCientifica Argentina 1936 122 288ndash96

74 GraysonDKMeltzer DJ Clovis hunting and large mammal extinctiona critical review of the evidence J World Prehist 2002 16 313ndash59doi101023A1022912030020

75 Haller H Der Rothirsch im Schweizerischen Nationalpark und dessenUmgebung Eine alpine population von Cervus elaphus zeitlich undraumlumlich dokumentiert Nationalpark-Forschung Schweiz 2002 911ndash144

76 Luccarini S Mauri L Ciuti S Lamberti P Apollonio M Reddeer (Cervus elaphus) spatial use in the Italian Alps home rangepatterns seasonal migrations and effects of snow and winterfeeding Ethol Ecol Evol 2006 18 127ndash45 doi1010800892701420069522718

77 Hornaday WT The extermination of the American bison Report USNational Museum The Smithsonian Institution Washington DCGovernment Printing Office 1889

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80 Fairbanks WS Bailey JA Cook RS Habitat use by a low-elevationsemicaptive bighorn sheep population J Wildl Manage 1987 51912ndash5 doi1023073801759

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82 Miracle P SturdyDChamois and theKarst ofHerzegovina J ArchaeolSci 1991 18 89ndash108 doi1010160305-4403(91)90080-9

83 Phoca-Cosmetatou N Site function and the lsquoibex-site phenomenonrsquomyth or realityOxf J Archaeol 2004 23 217ndash42 doi101111j1468-00922004t01-1-00210x

338 Animal Production Science W T Flueck and J M Smith-Flueck

84 Phoca-Cosmetatou N Landscape use in Northeast Italy during theUpper Palaeolithic Preistoria Alpina 2005 41 23ndash49

85 Molinari-Jobin A Molinari P Breitenmoser-Wursten C BreitenmoserU Significance of lynx Lynx lynx predation for roe deer Capreoluscapreolus and chamoisRupicapra rupicapramortality in the Swiss JuraMountains Wildl Biol 2002 8 109ndash15

86 Baumann M Babota C Schibler J Native or naturalized ValidatingAlpine chamois habitat models with archaeozoological data Ecol Appl2005 15 1096ndash110 doi10189002-5184

87 Choisy JP Reintroduction de bouqetins Capra sp conditions dereussite choix de massifs enseignements Lrsquoexample du VercorsJournal of Mountain Ecology 1994 2(Suppl) 15ndash33

88 Phoca-Cosmetatou N A zooarchaeological reassessment of the habitatand ecology of the ibex (Capra ibex) In Lauwerier RC Plug I editorsThe future from the past UK Oxbow Books 2004 pp 64ndash78

89 Lyman RL Paleozoology in the service of conservation biologyEvol Anthropol 2006 15 11ndash9 doi101002evan20083

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92 Smith-Flueck JM Barrio J Ferreyra N Nuntildeez A Tomas N Guzman JFlueck WT Hinojosa A Vidal F Garay G Jimenez J Advances inecology and conservation of Hippocamelus species in South AmericaAnim Prod Sci 2011 51 378ndash83 doi101071AN10287

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94 Kuzyk GW Dehn MM Farnell RS Body-size comparisons of alpine-and forest-wintering woodland caribou herds in the Yukon Can J Zool1999 77 1017ndash24 doi101139cjz-77-7-1017

95 Kojola I Huitu O Toppinen K Heikura K Heikkinen S Ronkainen SPredation on European wild forest reindeer (Rangifer tarandus) bywolves (Canis lupus) in Finland J Zool 2004 263 229ndash35doi101017S0952836904005084

96 Klein DR Meldgaard M Fancy SG Factors determining leg length inRangifer tarandus J Mammal 1987 68 642ndash55 doi1023071381597

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98 Parker KL Robbins CT Hanley TA Energy expenditures forlocomotion by mule deer and elk J Wildl Manage 1984 48 474ndash88doi1023073801180

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101 Turner CH Three rules for bone adaptation tomechanical stimuliBone1998 23 399ndash407 doi101016S8756-3282(98)00118-5

102 Kokshenev VB Silva JKL Garcia GJM Long-bone allometry ofterrestrial mammals and the geometric-shape and elastic-forceconstraints of bone evolution J Theor Biol 2003 224 551ndash6doi101016S0022-5193(03)00190-5

103 Kokshenev VB Christiansen P Salient features in the locomotion ofproboscideans revealed via the differential scaling of limb long bonesBiol J Linn Soc Lond 2010 100 16ndash29 doi101111j1095-8312201001415x

104 Ruff CBMechanical determinants of bone form insights from skeletalremains J Musculoskelet Neuronal Interact 2005 5 202ndash12

105 McKelvey KS AaubryKB SchwartzMK Using anecdotal occurrencedata for rare or elusive species the illusion of reality and a call forevidentiary standards Bioscience 2008 58 549ndash55 doi101641B580611

106 Fedosenko AK Blank DA Ovis ammon Mamm Species 2005 7731ndash15 doi1016441545-1410(2005)773[0001OA]20CO2

Manuscript received 10 September 2010 accepted 15 October 2010

Osteology of appendicular skeletons in Patagonian huemul Animal Production Science 339

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