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Phylogeny,classification,andevolutionaryecologyoftheCanidaeCHAPTERJANUARY2004
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Studies and reconstructions of dire wolf (Canis dirus) and Grey
wolf (Canis lupus) from late Pleistocene Rancholebrea Tarpits,Los
Angeles, California. Illustration by Pat Ortega.
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The evolutionary history of canids (Family Canidae)is a history
of successive radiations repeatedly occu-pying a broad spectrum of
niches ranging from large,pursuit predators to small omnivores, or
even to her-bivory. Three such radiations were first recognized
byTedford (1978), each represented by a distinct sub-family (Fig.
2.1). Two archaic subfamilies, Hespero-cyoninae and Borophaginae,
thrived in the middleto late Cenozoic from about 40 to 2 million
yearsago (Ma) (Wang 1994; Wang et al. 1999). All livingcanids
belong to the final radiation, SubfamilyCaninae, which achieved
their present diversity onlyin the last few million years (Tedford
et al. 1995).
Canids originated more than 40 Ma in the lateEocene of North
America from a group of archaic car-nivorans, the Miacidae (Wang
and Tedford 1994,1996). They were confined to the North
Americancontinent during much of their early history, play-ing a
wide range of predatory roles that encompassthose of the living
canids, procyonids, hyaenids, andpossibly felids. By the latest
Miocene (about 78 Ma),members of the Subfamily Caninae were finally
ableto cross the Bering Strait to reach Europe (Crusafont-Pair
1950), commencing an explosive radiation andgiving rise to the
modern canids of the Old World. Atthe formation of the Isthmus of
Panama, 3 Ma,canids arrived in South America and quickly
estab-lished themselves as one of the most diverse groupsof
carnivorans on the continent (Berta 1987, 1988).With the aid of
humans, Canis lupus dingo was trans-ported to Australia late in the
Holocene. Since thattime, canids have become truly worldwide
predators,unsurpassed in distribution by any other group
ofcarnivorans.
Here, in the context of this volume on the moderncanids, we
place more emphasis on the subfamilyCaninae, the latest of the
three successive radiationsof the Canidae. We do not attempt to
cite all of thereferences in canid palaeontology and
systematics,most of which have been summarized in the papersthat we
cite at the end of each section. Certain phy-logenetic
relationships of the Caninae are controver-sial, as reflected in
the different conclusions reachedon the basis of evidence from
palaeontological/morphological or molecular research as
presentedbelow.
What is a canid?Canids possess a pair of carnassial teeth (the
upperfourth premolar and lower first molar) in the form ofa
shearing device, and thus belong to the OrderCarnivora. Within the
Carnivora, canids fall into the Suborder Caniformia, or dog-like
forms. TheCaniformia are divided into two major groups thathave a
sister relationship: Superfamily Cynoidea,which includes Canidae,
and Superfamily Arctoidea,which include the Ursidae, Ailuridae,
Procyonidae,and Mustelidae, as well as the aquatic Pinnipediaand
the extinct Amphicyonidae.
As a cohesive group of carnivorans, living canidsare easily
distinguished from other carnivoran fami-lies. Morphologically
there is little difficulty in rec-ognizing living canids with their
relatively uniformand unspecialized dentitions. However, the canids
asexemplified by the living forms are narrowly defined.Only a small
fraction of a once diverse group has
CHAPTER 2
AncestryEvolutionary history, molecular systematics,
andevolutionary ecology of Canidae
Xiaoming Wang, Richard H. Tedford, Blaire Van Valkenburgh,and
Robert K. Wayne
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38 Biology and conservation of wild canids
3236
Orel-lan
Chad-ronian
Arikareean
Miocene Pliocene
Barstovian Claren-donian Blancan Irv.RLB
Pleist.+Holo.
HemphillianHeming-fordian
Whit-neyan
OligoceneEocene
28
RhizocyonOtarocyon
Archaeocyon
Hesperocyon
Paraenhydrocyon
Mesocyon
Cynodesmus
Caedocyon
Enhydrocyon
EctopocynusOsbornodon
SunkahetankaPhilotrox
Cynarctoides
Cormocyon
Phlaocyon
DesmocyonParacynarctus
MetatomarctusEuoplocyon
PsalidocyonProtomarctusTephrocyon
TomarctusAelurodonParatomarctus
CarpocyonProtepicyon
Leptocyon
New genus
VulpiniCanini
Vulpes
Eucyon
S. Am. caninesCaninae
BorophaginaeHesperocyoninae
UrocyonOtocyon
Xenocyon
Jackal-like CanisCoyote-like Canis
Wolf-like Canis
Cuon
Lycaon
Epicyon
Cynarctus
Oxetocyon
24 20 16 12 8EEEEEE LLLLLLM
4 Ma
3236 28 24 20 16 12 8 4 Ma
Borophagus
Figure 2.1 Simplified phylogenetic relationships of canids at
the generic level. Species ranges are indicated by individual bars
enclosed within grey rectangles, detailed relationships among
species in a genus is not shown. Relationships for
theHesperocyoninae is modified from Wang (1994, fig. 65), that for
the Borophaginae from Wang et al. (1999, fig. 141), and that for
the Caninae from unpublished data by Tedford et al.
Zubir-02.qxd 20#12#03 7:29 PM Page 38
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survived to the present day (Fig. 2.1). Canids in thepast had
departed from this conservative pattern suf-ficiently that
paleontologists had misjudged somecanids as procyonids. Similarly
the extinct bear-dog Family Amphicyonidae, which belongs to
theArctoidea, is often placed within the Canidae,because of its
unspecialized dentition.
How do we know a canid when we see one? A keyregion of the
anatomy used to define canids is themiddle ear region, an area that
distinguishes mostfamilies of carnivorans (Hunt 1974), perhaps as a
result of a widespread trend of ossifying bullarelements in
independent lineages. Canids are char-acterized by an inflated
entotympanic bulla that isdivided by a partial septum along the
entotympanicand ectotympanic suture (Fig. 2.2). Other
featurescharacteristic of canids is the loss of a stapedial
arteryand the medial position of the internal carotid artery that
is situated between the entotympanic and petrosal for most of its
course and contained within the rostral entotympanic anteriorly
(Wangand Tedford 1994). These basicranial character-istics have
remained more or less stable through-out the history of canids,
allowing easy identificationin the fossil record when these
structures arepreserved.
Evolutionary historyAmong the living families within the Order
Carnivora,the Canidae are the most ancient. The family arose inthe
late Eocene, when no other living families ofcarnivorans had yet
emerged (two archaic families,Miacidae and Viverravidae, have a
much older his-tory but none survive to the present time).
Further-more, canids still maintain some features that areprimitive
among all carnivorans, to the extent thatdog skulls are often used
to illustrate a generalizedmammal in zoological classrooms.
Dentally, canidsare closest to the ancestral morphotype of
Carnivora.Canids have a relatively unreduced dental formula
of3142/3143 [numbers in sequence represent incisors,canines,
premolars, and molars in the upper (left halfbefore the oblique)
and the lower (right half after theoblique) teeth] and relatively
unmodified molarsexcept for the morphology of the carnassials (P4,
m1)typical of all carnivorans. In contrast, all other car-nivoran
families generally have a more reduceddental formula and highly
modified cusp patterns.
From this mesocarnivorous (moderately carniv-orous) conservative
plan, canids generally evolvetowards a hypercarnivorous (highly
carnivorous) orhypocarnivorous (slightly carnivorous) dental
pat-tern. In the hypercarnivorous pattern (Fig. 2.4(b,d) )
Ancestry 39
Bullar septum
Ectotympanic
Caudal entotympanicInternal carotid artery
Anterior
Dorsal
PetrosalLa
tera
l
Figure 2.2 Ventrolateral view ofbasicranial morphology of
aprimitive canid, Hesperocyongregarius, showing bullarcomposition
and position of theinternal carotid artery (see text
forexplanations). The ventral floor ofthe bulla is dissected
away(isolated oval piece on top) toreveal the middle ear
structuresinside the bulla and the internalseptum. Modified from
Wang andTedford (1994, fig. 1).
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40 Biology and conservation of wild canids
Hesperocyon
Leptocyon
Tribe C
aniniTr
ibe
Vulp
ini
DesmocyonCynarctoides
Phlaocyon
Euoplocyoncyon
Cynodesmus
Osbornodon
Paraenhydrocyon
Hesperocyonnaei
Caninae
Borop
hagin
ae
5 5
10 10
15 15
20 20
25 25
30Ma
30Ma
Enhydrocyon
Cynarctus
Paratomar
Aelurodon
Carpocyon
Epicyon
P4 M1 M2
Vulpes
Eucyon
Cerdocyon
Urocyon
CuonCanisS. Am. canines
Canis clade
Borophagus
Vulpes clade
Figure 2.3 Dental evolution of representative canids as shown in
upper cheek teeth (P4M2). Generally the most derivedspecies in each
genus is chosen to enhance a sense of dental diversity. Species in
the Hesperocyoninae are: Hesperocyongregarius; Paraenhydrocyon
josephi; Cynodesmus martini; Enhydrocyon crassidens; and Osbornodon
fricki. Species in theBorophaginae are: Cynarctoides acridens;
Phlaocyon marslandensis; Desmocyon thomsoni; Cynarctus crucidens;
Euoplocyonbrachygnathus; Aelurodon stirtoni; Paratomarctus
temerarius; Carpocyon webbi; Epicyon haydeni; and Borophagus
diversidens.Species in the Caninae are: Leptocyon gregorii; Vulpes
stenognathus; Urocyon minicephalus; Cerdocyon thous; Eucyon
davisi;Canis dirus; and Cuon alpinus. All teeth are scaled to be
proportional to their sizes.
there is a general tendency to increase the size of
thecarnassial pair at the expense of the molars behind (see
Enhydrocyon, Aelurodon, Borophagus, and Cuon inFig. 2.3). This
modification increases the efficiencyof carnassial shear. A
hypocarnivorous pattern(Fig. 2.4(a,c) ) is the opposite, with
development of thegrinding part of the dentition (molars) at the
expenseof carnassial shear (see Cynarctoides, Phlaocyon,
andCynarctus in Fig. 2.3). This configuration was only pos-sible in
the sister-taxa Borophaginae and Caninae,which share a bicuspid m1
talonid (Fig. 2.4(c) ). One ofthe major trends in canid evolution
is the repeated
development of hyper- and hypocarnivorous forms(see below).
HesperocyoninaeThe Subfamily Hesperocyoninae is the first
majorclade with a total of 28 species. Its earliest membersare
species of the small fox-like form, Hesperocyon,that first appears
in the late Eocene (Duchesnean,3740 Ma) (Bryant 1992) and became
abundant inthe latest Eocene (Chadronian). By Oligocene time
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(Orellan and Whitneyan, 3430 Ma), early membersof four small
clades of the hesperocyonines hademerged: Paraenhydrocyon,
Enhydrocyon, Osbornodon,and Ectopocynus. Hesperocyonines
experienced theirmaximum diversity of 14 species during the
lateOligocene (early Arikareean in 3028 Ma), and
reached their peak predatory adaptations (hypercar-nivory) in
the earliest Miocene (late Arikareean) withadvanced species of
Enhydrocyon and Paraenhydrocyon.The last species of the subfamily,
Osbornodon fricki,became extinct in the early Barstovian (15 Ma),
reach-ing the size of a small wolf.
Ancestry 41
ProtoconeProtocone
Parastyle
P4M1
M2
ParastyleParacone Paracone
Metacone
TalonidHypoconidProtoconid
Paraconid
Hypoconid
Talonid
Entoconid
Protoconid
Protostylid
Paraconid
Metaconid
m1 m2m3
ProtoconeProtocone
Parastyle
Metacone
Hypocone
Hypocone
Paracone(a) (b)
(c) (d)
Figure 2.4 Hypercarnivorous (b, Aelurodon and d, Euoplocyon) and
hypocarnivorous (a, Phlaocyon and c, Cynarctus) dentitions.
Inhypercarnivorous forms, the upper cheek teeth (b) tend to
emphasize the shearing part of the dentition with an elongated
andnarrow P4, an enlarged parastyle on a transversely elongated M1,
and a reduced M2. On the lower teeth (d), hypercarnivory
isexemplified by a trenchant talonid due to the increased size and
height of the hypoconid at the expense of the entoconid (reducedto
a narrow and low ridge), accompanied by the enlargement of the
protoconid at the expense of the metaconid (completely lost
inEuoplocyon) and the elongation of the trigonid at the expense of
the talonid. In hypocarnivorous forms, on the other hand, the
upperteeth (a) emphasize the grinding part of the dentition with a
shortened and broadened P4 (sometimes with a hypocone along
thelingual border), a reduced parastyle on a quadrate M1 that has
additional cusps (e.g. a conical hypocone along the
internalcingulum) and cuspules, and an enlarged M2. The lower teeth
(c) in hypocarnivorous forms possess a basined (bicuspid) talonid
onm1 enclosed on either side by the hypoconid and entoconid that
are approximately equal in size. Other signs of hypocarnivory on
thelower teeth include widened lower molars, enlarged metaconids,
and additional cuspules such as a protostylid.
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With the exception of the Osbornodon clade, whichacquired a
bicuspid m1 talonid, hesperocyonines areprimitively
hypercarnivorous in dental adaptationswith tendencies towards
reduced last molars andtrenchant (single cusped) talonid heels on
the lowerfirst molar. Although never reaching the extremesseen in
the borophagines, hesperocyonines hadmodest development of bone
cracking adaptationsin their strong premolars. At least three
lineages, inall species of Enhydrocyon and in terminal species
ofOsbornodon and Ectopocynus, have independentlyevolved their own
unique array of bone crackingteeth. Hesperocyonines did not
experiment withhypocarnivory.
Members of this subfamily were the topic of amonograph by Wang
(1994). Two additional speciesof Osbornodon have since been added
to the subfam-ily (Hayes 2000; Wang in press). The
evolutionarytransition from plantigrade to digitigrade
standingposture in early canids was explored by Wang (1993).A
hereditary condition, osteochondroma, in thepostcranials of early
canids was documented byWang and Rothschild (1992).
BorophaginaeFrom the primitive condition of a trenchant
talonidheel on the lower first molar seen in the hesperocyo-nines,
borophagines, and canines shared a basined(bicuspid) talonid
acquired at the very beginning oftheir common ancestry (Fig. 2.4(c)
). Along with amore quadrate upper first molar with its
hypocone,the basined talonid establishes an ancestral statefrom
which all subsequent forms were derived. Sucha dental pattern
proved to be very versatile andcan readily be adapted towards
either a hyper- orhypocarnivorous type of dentition, both of
whichwere repeatedly employed by both borophaginesand canines (Fig.
2.3).
The history of the borophagines also begins witha small fox-like
form, Archaeocyon, in the late Oligo-cene. Contemporaneous with
larger and more pre-datory hesperocyonines, these early
borophagines in the late Oligocene and early Miocene
(Arikareean)tended to be more omnivorous (hypocarnivorous) intheir
dental adaptations, such as Oxetocyon, Otarocyon,and Phlaocyon. One
extreme case, Cynarctoides evolved
selenodont-like molars as in modern artiodactyles,a rare
occurrence of herbivory among carnivorans.These early borophagines
are generally no largerthan a raccoon, which is probably a good
ecologicalmodel for some borophagines at a time when procy-onids
had yet to diversify.
After some transitional forms in the early
Miocene(Hemingfordian), such as Cormocyon and
Desmocyon,borophagines achieved their maximum ecologicaland
numerical (i.e. species) diversity in the middleMiocene
(Barstovian), with highly omnivorousforms, such as Cynarctus, that
were almost ursid-like aswell as highly predatory forms, such as
Aelurodon, thatwere a larger version of the living African
HuntingDog Lycaon. By then, borophagines had acquiredtheir unique
characteristics of a broad muzzle, a bonycontact between
premaxillary and frontal, multi-cuspid incisors, and an enlarged
parastyle on theupper carnassials (modified from an enlargement
ofthe anterior cingulum).
By the end of the Miocene, borophagines hadevolved another
lineage of omnivory, although onlymodestly in that direction, in
the form of Carpocyon.Species of Carpocyon are mostly the size of
jackals tosmall wolves. At the same time, the emergence of thegenus
Epicyon from a Carpocyon-like ancestor markedanother major clade of
hypercarnivorous boro-phagines. The terminal species of Epicyon, E.
haydeni,reached the size of a large bear and holds record asthe
largest canid ever to have lived (Fig. 2.5). Closelyrelated to
Epicyon is Borophagus, the terminal genusof the Borophaginae. Both
Epicyon and Borophagusare best known for their massive P4 and p4 in
con-trast to the diminutive premolars in front. This pairof
enlarged premolars is designed for cracking bones,mirroring similar
adaptations by hyaenids in the OldWorld. Advanced species of
Borophagus survived thePliocene but became extinct near the
beginning ofthe Pleistocene.
The phylogeny and systematics of the Boropha-ginae were recently
revised by Wang et al. (1999),which is the basis of above summary.
Munthe (1979,1989, 1998) analysed the functional morphology
ofborophagine limb bones and found a diverse arrayof postcranial
adaptations, in contrast to the morestereotypical view that the
hyaenoid dogs were non-cursorial scavengers only. Werdelin (1989)
compared
42 Biology and conservation of wild canids
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the bone-cracking adaptations of borophagine canidsand hyaenids
in terms of evolutionary constraintswithin their prospective
lineages.
CaninaeAs in the hesperocyonines and borophagines, a small
fox-sized species of Leptocyon is the earliestrecognized member of
the subfamily Caninae. Besidessharing a bicuspid talonid of m1 and
a quadrate M1with the borophagines, Leptocyon is also
character-ized by a slender rostrum and elongated lower jaw,and
correspondingly narrow and slim premolars,features that are
inherited in all subsequent canines.It first appeared in the early
Oligocene (Orellan) andpersisted through the late Miocene
(Clarendonian).Throughout its long existence (no other canid
genushad as long a duration), facing intense competitionfrom the
larger and diverse hesperocyonines andborophagines, Leptocyon
generally remains smalland inconspicuous, never having more than
two orthree species at a time.
By the latest Miocene (Hemphillian), fox-sizedniches are widely
available in North America, leftopen by extinctions of all small
borophagines. Thetrue fox clade, Tribe Vulpini, emerges at this
time andundergoes a modest diversification to initiate primit-ive
species of both Vulpes and Urocyon (and theirextinct relatives).
The North American Pliocenerecord of Vulpes is quite poor.
Fragmentary materials
from early Blancan indicate the presence of a SwiftFox-like form
in the Great Plains. Vulpes species werewidespread and diverse in
Eurasia during thePliocene (see Qiu and Tedford 1990), resulting
froman immigration event independent from that of theCanis clade.
Red Fox (Vulpes vulpes) and Arctic Fox(Vulpes lagopus) appeared in
North America onlyin the late Pleistocene, evidently as a result of
animmigration back to the New World.
Preferring more wooded areas, the grey fox Urocyonhas remained
in southern North America and MiddleAmerica. Records of the grey
fox clade have a more or less continuous presence in North
Americathroughout its existence, with intermediate formsleading to
the living species Urocyon cinereoargenteus.Morphologically, the
living African Bat-eared FoxOtocyon is closest to the Urocyon
clade, althoughmolecular evidence suggests that the Bat-eared
Foxlies at the base of the fox clade or even lower (Geffenet al.
1992d; Wayne et al. 1997). If the morphologicalevidence has been
correctly interpreted, then theBat-eared fox must represent a
Pliocene immigrationevent to the Old World independent of other
foxes.A transitional form, Protocyon, occurs in southernAsia and
Africa in the early Pleistocene.
Advanced members of the Caninae, Tribe Canini,first occur in the
medial Miocene (Clarendonian,912 Ma) in the form of a transitional
taxon Eucyon.As a jackal-sized canid, Eucyon is mostly
distin-guished from the Vulpini in an expanded paroccipi-tal
process and enlarged mastoid process, and in the
Ancestry 43
25 cm
Figure 2.5 Reconstruction ofEpicyon saevus (small
individual,based on AMNH 8305) andEpicyon haydeni (large
individual,composite figure, based onspecimens from Jack
SwayzeQuarry). These two species co-occur extensively during the
lateClarendonian and earlyHemphillian of Western NorthAmerica.
Illustration by MauricioAntn. (From Wang et al. 1999.)
Zubir-02.qxd 20#12#03 7:30 PM Page 43
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consistent presence of a frontal sinus. The lattercharacter
initiates a series of transformations in theTribe Canini
culminating in the elaborate develop-ment of the sinuses and a
domed skull in C. lupus. Bylatest Miocene time, species of Eucyon
have appearedin Europe (Rook 1992) and by the early Pliocene inAsia
(Tedford and Qiu 1996). The North Americanrecords all predate the
European ones, suggestinga westward dispersal of this form.
Arising from about the same phylogenetic level asEucyon is the
South American clade. Morphologicaland molecular evidence generally
agrees that livingSouth American canids, the most diverse group
ofcanids on a single continent, belong to a naturalgroup of their
own. The South American canids areunited by morphological
characters such as a longpalate, a large angular process of the jaw
with awidened scar for attachment of the inferior branch ofthe
medial pterygoid muscle, and a relatively longbase of the coronoid
process (Tedford et al. 1995).By the close of the Miocene, certain
fragmentarymaterials from southern United States and Mexicoindicate
that taxa assignable to Cerdocyon (Torres andFerrusqua-Villafranca
1981) and Chrysocyon occurin North America. The presence of these
derived taxain the North American late Miocene predicts
thatancestral stocks of many of the South Americancanids may have
been present in southern NorthAmerica or Middle America. They
appear in the SouthAmerican fossil record shortly after the
formation ofthe Isthmus of Panama in the Pliocene, around 3
Ma(Berta 1987). The earliest records are Pseudalopex andits close
relative Protocyon, an extinct large hyper-carnivore, from the
Pliocene (Uquian, around2.51.5 Ma) of Argentina. By the latest
Pleistocene(Lujanian, 300,00010,000 years ago), most livingspecies
or their close relatives have emerged, alongwith the extinct North
American Dire Wolf, Canisdirus. By the end of the Pleistocene, all
large, hyper-carnivorous canids of South America
(Protocyon,Theriodictis) as well as C. dirus had become
extinct.
The Canis clade within the Tribe Canini, the mostderived group
in terms of large size and hypercar-nivory, arises near the
MiocenePliocene boundarybetween 5 and 6 Ma in North America. A
series ofjackal-sized ancestral species of Canis thrived in
theearly Pliocene (early Blancan), such as Canis ferox,Canis
lepophagus, and other undescribed species. At
about the same time, first records of canids begin toappear in
the European late Neogene: Canis cipio inthe late Miocene of Spain
(Crusafont-Pair 1950),Eucyon monticinensis in the latest Miocene of
Italy(Rook 1992), the earliest raccoon-dog Nyctereutesdonnezani,
and the jackal-sized Canis adoxus in theearly Pliocene of France
(Martin 1973; Ginsburg1999). The enigmatic Canis cipio, only
representedby parts of the upper and lower dentition, may per-tain
to a form at the Eucyon level of differentiationrather than truly a
species of Canis.
The next phase of Canis evolution is difficult totrack. The
newly arrived Canis in Eurasia underwentan extensive radiation and
range expansion in thelate Pliocene and Pleistocene, resulting in
multiple,closely related species in Europe, Africa, and Asia.
Tocompound this problem, the highly cursorial wolf-like Canis
species apparently belong to a circum-arcticfauna that undergoes
expansions and contractionswith the fluctuating climate.
Hypercarnivorousadaptations are common in the crown-group ofspecies
especially in the Eurasian middle latitudesand Africa. For the
first time in canid history, phylo-genetic studies cannot be
satisfactorily performed onforms from any single continent because
of theirHolarctic distribution and faunal interminglingbetween the
new and old worlds. Nevertheless someclades were localized in
different parts of Holarctica.The vulpines major centre of
radiation was in theOld World. For the canines, North America
remaineda centre through the Pliocene producing the Coyoteas an
endemic form. A larger radiation yielding thewolves, dhole, African
hunting dog, and fossil relat-ives took place on the Eurasian and
African conti-nents. During the Pleistocene elements of the
largercanid fauna invaded mid-latitude North Americathe last
invasion of which was the appearance of theGrey wolf south of the
glacial ice sheets in the latestPleistocene (about 100 Ka).
A comprehensive systematic revision of NorthAmerican fossil
canines by Tedford et al. (in pre-paration) forms the basis of much
of the foregoingsummary. As part of that revision, the
phylogeneticframework as derived from living genera waspublished by
Tedford et al. (1995). Nowak (1979)published a monograph on the
Quaternary Canis ofNorth America. Berta (1981, 1987, 1988)
undertookthe most recent phylogenetic analysis of the South
44 Biology and conservation of wild canids
Zubir-02.qxd 20#12#03 7:30 PM Page 44
-
American canids. Rook (1992, 1994) and Rook andTorre (1996a,b)
partially summarized the Eurasiancanids. The African canid records
are relatively poorly understood but recent discoveries promise
toadvance our knowledge in that continent (Werdelin,personal
communication). See also citations belowfor recent molecular
systematic studies.
Molecular systematicsThe ancient divergence of dogs from other
carnivores is reaffirmed by molecular data. DNADNA hybridization of
single copy DNA clearly shows them as the first divergence in the
suborderCaniformia that includes seals, bears, weasel,
andraccoon-like carnivores (Fig. 2.6). This basal place-ment is
further supported by mitochondrial DNAsequence studies (Vrana et
al. 1994; Slattery andBrien 1995; Flynn and Nedbal 1998), and
recentlystudies of DNA sequences from nuclear genes(Murphy et al.
2001). Based on molecular clockcalculations, the divergence time
was estimated as 50 million years before present (Wayne et al.
1989).This value is consistent with the first appearance ofthe
family in the Eocene, although it is somewhatmore ancient than the
date of 40 million years sug-gested by the fossil record (see
above). Consideringthat first appearance dates generally post-date
actualdivergence dates because of the incompleteness of therecord
(e.g. Marshall 1977), the agreement betweenfossil and molecular
dates is surprisingly good.
Evolutionary relationships within the familyCanidae have been
reconstructed using comparativekaryology, allozyme electrophoresis,
and mitochon-drial DNA protein coding sequence data (Wayne andBrien
1987; Wayne et al. 1997, 1987a,b). Further,relationships at the
genus level have been studiedwith mtDNA control region sequencing
(a non-coding, hypervariable segment of about 1200 bp inthe
mitochondrial genome) and microsatellite loci(hypervariable single
copy nuclear repeat loci)(Geffen et al. 1992; Bruford and Wayne
1993; Girmanet al. 1993; Gottelli et al. 1994; Vil et al. 1997,
1999).The protein-coding gene phylogeny, which is largelyconsistent
with trees based on other genetic approaches, shows that the wolf
genus Canis is amonophyletic group that also includes the Dhole
orAsian Wild Dog (Cuon alpinus). The Grey wolf, coyote
Ancestry 45
Dog
Jackal
Arctic fox
Spotted shunk
Striped skunk
Mink
Weasel
Ferret
Otter
Raccoon
Red panda
Brown bear
Malayan sun bear
Spectacled bear
Giant panda
Harbor seal
Sea lion
Walrus
Spotted genet
Civet
Palm civet
Mongoose
Spotted hyena
Domestic cat
Jungle cat
Ocelot
Geoffroey cat
Lion
Leopard
Cheetah
Striped hyena
1020304050
MYBP
Felidae
Hyaenidae
Herpestidae
Viverridae
Odobenidae
Feliformia
Caniformia
OlariidaePhocidae
Ursidae
Procyonidae
Mustelidae
Mephitidae
Canidae
Figure 2.6 Relationship of carnivores based on DNAhybridization
data (Wayne et al. 1989). Family and suborder groupings are
indicated. Time scale in millions ofyear before present (MYBP) is
based on comparisons of DNAsequence divergence to first appearance
times in the fossilrecord.
Zubir-02.qxd 20#12#03 7:30 PM Page 45
-
(Canis latrans) and Ethiopian wolf (Canis simensis)form a
monophyletic group, with the Golden Jackal(C. aureus) as the most
likely sister taxon (Fig. 2.7). TheBlack-backed and Side-striped
jackals are sister taxa,but they do not form a monophyletic group
with theGolden jackal and Ethiopian wolf. Basal to Canis and
Cuon are the African hunting dog (Lycaon pictus) and aclade
consisting of two South American canids, thebush dog (Speothos
venaticus) and the maned wolf(Chrysocyon brachyurus). Consequently,
although theAfrican hunting dog preys on large game as does theGrey
wolf and dhole, it is not closely related to either
46 Biology and conservation of wild canids
Harbor sealIsland grey fox
Grey foxRaccoon dog
Bat-eared fox
Fennec fox
Red foxKit fox
Arctic fox
Grey wolf
Coyote
Ethiopian wolf
Golden jackal
Black-backed jackal
Dhole
Side-striped jackal
Crab-eatingfox
Argentine grey foxDarwins fox
Culpeo fox
Hoary fox
Pampas fox
Sechuran fox
Small-eared dog
MYBP
Bush dog
Maned wolf
African hunting dog
Red fox-likecanids
Wolf-likecanids
SouthAmericanfoxes
10 6 2
Figure 2.7 Consensus tree of 26 canid species based on analysis
of 2001 bp of DNA sequence from mitochondrial proteincoding genes
(Wayne et al. 1997). See Geffen et al. (1992) for a more detailed
analysis of the Red-fox like canids. Time scale in millions of year
before present (MYBP) is based on comparisons of DNA sequence
divergence to first appearance times in the fossil record.
Zubir-02.qxd 20#12#03 7:30 PM Page 46
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Ancestry 47
species but is sister to the clade containing thesespecies. This
phylogeny implies that the trenchantheeled carnassial now found
only in Speothos, Cuon,and Lycaon, evolved at least twice or was
primitive andlost in other wolf-like canids and the maned wolf.
The South American canids do not form a mono-phyletic group.
Speothos and Chrysocyon are sister taxathat group with the
wolf-like canids rather than theSouth American foxes. The large
sequence divergencebetween the bush dog and maned wolf and
betweenthese taxa and the South American foxes suggeststhat they
diverged from each other 67 Ma, wellbefore the Panamanian land
bridge formed about23 Ma. Thus, three canid invasions of
SouthAmerica are required to explain the phylogeneticdistribution
of the extant species. These invasions are today survived by (1)
the bush dog, (2) the manedwolf, and (3) the South American foxes.
Further,within the South American foxes, divergence valuesbetween
crab-eating fox (Cerdocyon thous), the Short-eared fox (Atelocynus
microtis), and other SouthAmerican foxes, suggest they may have
divergedbefore the opening of the Panamanian land bridge aswell
(Wayne et al. 1997). The fossil record supportsthe hypothesis that
the crab-eating fox had its origin outside of South America, as the
genus hasbeen described from late Miocene deposits of NorthAmerica
(36 Ma) (Berta 1984, 1987, see above).Consequently, only the foxes
of the genus Pseudalopex,Lycalopex, and perhaps Atelocynus, might
have aSouth American origin. Further, the generic distinc-tion
given to Pseudalopex and Lycalopex does not reflectmuch genetic
differentiation, and in the absence ofappreciable morphologic
differences, the geneticdata suggest these species should be
assigned to asingle genus.
A fourth grouping in the tree consists of other fox-like taxa,
including Vulpes, Alopex, and Fennecus(Fig. 2.7) (Geffen et al.
1992; Mercure et al. 1993;Wayne et al. 1997). The Arctic Fox,
Alopex, is a closesister to the Kit Fox, Vulpes macrotis and both
share thesame unique karyotype (Wayne et al. 1987a). Basal toVulpes
is Fennecus, suggesting an early divergence ofthat lineage.
Finally, Otocyon, Nyctereutes, and Urocyonappear basal to other
canids in all molecular and kary-ological trees (Wayne et al.
1987a). The first two taxaare monospecific whereas the third
includes theIsland Fox, Urocyon littoralis and the grey fox,
U. cinereoargenteus. The three genera diverged early inthe
history of the family, approximately 812 Ma assuggested by
molecular clock extrapolations.
In sum, the living Canidae is divided into fivedistinct
groupings. These include the wolf-like canids,which consists of the
Coyote, Grey wolf, Jackals,dhole, and African hunting dog. This
clade is associ-ated with a group containing bush dog and manedwolf
in some trees and further, this larger grouping isassociated with
the South American foxes (Wayne et al. 1997). The Red Fox group is
a fourth independentclade containing Alopex, Vulpes, and
Fennecus.Finally, three lineages have long distinct
evolutionaryhistories and are survived today by the Raccoon
Dog,Bat-eared Fox, and grey fox. Assuming an approxi-mate molecular
clock, the origin of the modernCanidae begins about 1012 Ma and is
followed bythe divergence of wolf and fox-like canids about6 Ma.
The South American canids are not a mono-phyletic group and likely
owe their origin to threeseparate invasions. This group included
the manedwolf, bush dog, crab-eating fox, and the other
SouthAmerican canids, which diverged from each otherabout 36
Ma.
Morphological and molecularphylogeniesTedford et al. (1995)
performed a cladistic analysis ofliving canids on morphological
grounds. The result is a nearly fully resolved relationship based
on an 18 taxa by 57 characters matrix at the generic level.This
relationship recognizes three monophyleticclades in the canines:
the fox group (tribe Vulpini),the South American canine group, and
the wolfgroup containing hypercarnivorous forms (the lattertwo form
the tribe Canini). Recent molecular studies(presented above), on
the other hand, contradictsome of these arrangements while
maintaining otherparts in the morphological tree (Fig. 2.8(a)
).
Trees derived from 2001 bp of mitochondrial DNA(Wayne 1997, p.
239 and Fig. 2.7 of this chapter) tendto places the foxes near the
basal part, the SouthAmerican canines in the middle, and the wolves
andhunting dogs towards the terminal branches, a pat-tern that is
consistent with the morphological tree.
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-
The detailed arrangements, however, differ in a num-ber of ways.
The foxes are generally in a paraphyleticarrangement in contrast to
a monophyletic clade inthe morphological tree. The grey fox and
bat-earedfox are placed at the base despite their highly
deriveddental morphology compared with other foxes.
Similarly, South American canines are no longermonophyletic
under molecular analysis but form atleast two paraphyletic
branches. A glaring discr-epancy is the Asiatic raccoon dog being
allied to thefoxes in the molecular analysis despite its
numerousmorphological characters shared with some South
48 Biology and conservation of wild canids
Vulp
es
Uroc
yon
Otoc
yon
Pse
udal
opex
Pseu
dalo
pex
Dusi
cyon
Lyca
lope
x
Chry
socy
on
Cerd
ocyo
n
Nyct
ereu
tes
Atel
ocyn
us
Speo
thos
Cani
s
Cuon
Lyca
on
Uroc
yon
Vulp
es
Otoc
yon
Nyct
ereu
tes
Speo
thos
Chry
socy
on
Cerd
ocyo
n
Atel
ocyn
us
Pseu
dalo
pex
Lyca
lope
x
Sech
uran
fox
Lyca
on
Cani
s
Cuon
Molecular tree(Wayne et al. 1997)
Morphological tree(Tedford et al. 1995)
Combined analysis(Wayne et al. 1997)
(a)
(b)
Figure 2.8 (a) Contrasting caninerelationships from recent
morphological(Tedford et al. 1995) and molecularstudies (Wayne et
al. 1997 and Fig. 2.7);(b) combined analysis of 2001 bp ofcanid
mtDNA and 57 morphologicalcharacters (Wayne et al. 1997, fig.
7).
Zubir-02.qxd 20#12#03 7:30 PM Page 48
-
Ancestry 49
American forms. Finally, molecular data suggestindependent
origins for the Asiatic and Africanhunting dogs in contrast to a
sister relationship inthe morphological tree supported by a large
numberof characters related to hypercarnivory.
Not surprisingly, there are increased agreementsbetween the
molecular and morphological resultswhen the two data sets are
combined in a total evi-dence analysis (Fig. 2.8(b) ). Under such
conditions,the South American canines (except Nyctereutes)become
monophyletic, as does the clade includingthe wolf, dhole, and
African hunting dog.
Evolutionary ecologyIterative evolution of hypercarnivoryOne of
the most remarkable features of canid historyis their repeated
tendency to evolve both hypocar-nivorous and hypercarnivorous
forms. As notedabove, hypercarnivorous species evolved within
eachsubfamily, and hypocarnivorous species evolvedwithin two of the
three (all but the Hesperocyo-ninae). Hypocarnivory was most fully
expressed inthe Borophaginae, where at least 15 species showed
atendency towards a dentition similar to that of livingraccoons
(Wang et al. 1999). Among the Caninae, thetendency has not been
quite as strong, with only asingle lineage, Nyctereutes, developing
a markedlyhypocarnivorous dentition. However, all three
sub-families include multiple species of apparent hyper-carnivores
with enhanced cutting blades on theircarnassials, reduced grinding
molars, and enlargedcanines and lateral incisors. When and why
didhypercarnivory evolve within each subfamily?
In two of the three subfamilies, Hesperocyoninaeand Caninae, the
evolution of hypercarnivoryappears to have occurred at least partly
in response toa reduced diversity of other hypercarnivorous
taxa.The Hesperocyoninae evolved hypercarnivory earlyin their
history (Figs 2.1 and 2.7) and the mostadvanced forms appear in the
early Miocene (about2420 Ma) at a time when the two previously
domi-nant carnivorous families had vanished. These twofamilies were
the Nimravidae, an extinct group ofsaber-tooth cat-like forms, and
the Hyaenodontidae,a group of somewhat dog-like predators included
in the extinct order Creodonta. The nimravids
and hyaenodontids dominated the North Americanguild of large,
predatory mammals in the late Eoceneto mid-Oligocene (3729 Ma), but
faded rapidly in thelate Oligocene, and were extinct in North
America byabout 25 Ma (Van Valkenburgh 1991, 1994). Duringmost of
their reign, hesperocyonines existed at lowdiversity and small
(fox-size) body size, but as thehyaenodontids and nimravids
declined in the lateOligocene, the early canids seem to have
radiated toreplace them. Most of these hypercarnivorous canidswere
jackal-size (less than 10 kg), with only the lastsurviving species,
Osbornodon fricki, reaching the sizeof a small wolf (Wang 1994). In
the early Miocene,large hypercarnivores immigrated from the
OldWorld in the form of hemicyonine bears (Ursidae) and
temnocyonine bear-dogs (Amphicyonidae). Thesubsequent decline to
extinction of the hesperocy-onines might have been a result of
competition withthese new predators (Van Valkenburgh 1991,
2001).
Hypercarnivory appears late in the history of theCaninae and
represents at least several independentradiations in South America,
North America, and theOld World (Figs 2.1 and 2.7). As was true of
the hes-perocyonine example, the South American radiationof large
hypercarnivorous canids occurred at a time(2.50.01 Ma) when
cat-like predators were rare orabsent. It followed the elevation of
the Panamanianland bridge around 23 Ma that allowed immigra-tion
between the previously separated continents.The canids that first
entered South America founda depauperate predator community,
consisting of onebear-like procyonid carnivoran, three species of
car-nivorous didelphid marsupials, one of which was thesize of a
coyote, and a gigantic, predaceous groundbird (Marshall 1977). With
the possible exception ofthe rare ground bird, none of these
species was aspecialized hypercarnivore. Between 2.5 Ma and10,000
years ago, 16 new species of canids appearedin South America, at
least seven of which had tren-chant heeled carnassials and clearly
were adapted forhypercarnivory (Berta 1988; Van Valkenburgh
1991).They represent three different endemic genera,Theriodictis,
Protocyon, and Speothos. In addition,there were three large
wolf-like species of Canis inSouth America, Canis gezi, Canis
nehringi, and Canisdirus, all of which were probably
hypercarnivorousbut retained a bicuspid heel on their carnassials.
Ofthese only the Dire Wolf, C. dirus, evolved in NorthAmerica. All
but one of these ten hypercarnivorous
Zubir-02.qxd 20#12#03 7:30 PM Page 49
-
canids of South America went extinct at the end ofthe
Pleistocene (Van Valkenburgh 1991). The solesurvivor, the bush dog
(Speothos) is rarely sighted.
In the Old World, the evolution of hypercarnivo-rous canines
occurred within the last 4 million yearsand did not coincide with
an absence of cats. Largecats, both sabertooth and conical tooth
forms, arepresent throughout the Plio-Pleistocene when thehighly
carnivorous species of Canis, Cuon, Lycaon,and Xenocyon appear
(Turner and Antn 1996).However, their evolution might be a response
to thedecline of another group of hypercarnivores, wolf-like
hyaenids. Hyaenids were the dominant dog-likepredators of the Old
World Miocene, reaching adiversity of 22 species between 9 and 5
Ma, but thendeclining dramatically to just five species by about4
Ma (Werdelin and Turner 1996). Their decline mayhave opened up
ecospace for the large canids andfavored the evolution of
hypercarnivory.
The remaining episode of hypercarnivory incanids occurred in the
Borophaginae between 15 and4 Ma (Van Valkenburgh et al. in press).
As was true ofthe Caninae, the hypercarnivorous species do
notevolve early in the subfamilys history. Instead, theyappear in
the latter half of the subfamilys lifespanand only become prevalent
in the last third (midlate Miocene; Figs 2.1 and 2.7). In the late
Miocene,
borophagine canids were the dominant dog-likepredators of North
America, having replaced theamphicyonids and hemicyonine bears that
hadthemselves replaced the hesperocyonines some tenmillion years
earlier (Van Valkenburgh 1999). In thecase of the Borophaginae, the
evolution of hyper-carnivory appears more gradual than in the
othertwo subfamilies, and is not easily ascribed to oppor-tunistic
and rapid evolution into empty ecospace.
In all three subfamilies, there is a pattern of
greaterhypercarnivory and increasing body size with time(Fig. 2.9).
Even in the Hesperocyoninae, where hyper-carnivory evolves very
early, large species with themost specialized meat-eating
dentitions appear later(Wang 1994). This directional trend towards
the evo-lution of large, hypercarnivorous forms is apparentin other
groups of dog-like carnivores, such asthe amphicyonids (Viranta
1996) and hyaenids(Werdelin and Solounias 1991; Werdelin and
Turner1996), and may be a fundamental feature of carni-vore
evolution. The likely cause is the prevalence ofinterspecific
competition among large, sympatricpredators. Interspecific
competition tends to bemore intense among large carnivores because
preyare often difficult to capture and can represent asizable
quantity of food that is worthy of stealing anddefending.
Competition appears to be a motive for
50 Biology and conservation of wild canids
0
10
20
30
40
0
5
10
15
0
10
20
30
40
50
N
Millions of years before present
Hesperocyoninae Borophaginae Caninae
3730 3022 2215 3424 2414 142 3423 2312 125 50
Figure 2.9 Iterative evolution of large hypercarnivores. Number
(N) of hypocarnivorous (white), mesocarnivorous (grey), and large
(20 kg) hypercarnivorous (black) species over time in each of the
three subfamilies. The few hesperocyonine species
withtrenchant-heeled carnassials estimated to have been less than
20 kg in mass were assigned to the mesocarnivorous categorybecause
they are assumed not have taken prey as large or larger than
themselves. For the Hesperocyoninae and Borophaginae,their
stratigraphic ranges were broken into thirds; for the Caninae, four
time divisions were used because of the large number ofspecies
appearing in the past 5 million years. Species were assigned to
dietary categories and body mass was estimated on thebasis of
dental morphology as described in Van Valkenburgh (1991) and Wang
et al. (1999).
Zubir-02.qxd 20#12#03 7:30 PM Page 50
-
The last one million yearsAll of the canids that are extant
today evolved wellprior to the late Pleistocene extinction event
approx-imately 11,000 years ago. The same could be said ofmost, if
not all, extant carnivores. In the New World,the end-Pleistocene
event removed numerous largemammals, including both herbivores
(e.g. camels,horses, proboscideans) and carnivores (e.g.
SabertoothCat, Dire Wolf, Short-faced Bear). In the Old World,many
of the ecological equivalents of these speciesdisappeared earlier,
around 500,000 years ago(Turner and Antn 1996). Consequently, all
extantcarnivore species evolved under very differentecological
circumstances than exist at present. Forexample, the Grey wolf
today is considered the toppredator in much of Holarctica, but it
has only heldthis position for the last ten to eleven thousand
years.For hundreds of thousands of years prior to that time,the
wolf coexisted with 11 species of predator as large or larger than
itself (Fig. 2.10). Now there arebut three, the Puma, Black Bear,
and Grizzly Bear, andwolves are usually dominant over the first two
speciesat least (Van Valkenburgh 2001). Thus, for most of
itsexistence, the Grey wolf was a mesopredator ratherthan a top
predator, and so its morphology andbehaviour should be viewed from
that perspective.Given the greater diversity and probable
greaterabundance of predators in the past, interspecificcompetition
was likely more intense than at pre-sent. Higher tooth fracture
frequencies in latePleistocene North American predators provide
indi-rect evidence of heavy carcass utilization and strongfood
competition at that time (Van Valkenburghand Hertel 1993). Intense
food competition wouldfavour group defence of kills and higher
levels ofinterspecific aggression. Perhaps the sociality of thewolf
and the tendency of some carnivores to kill butnot eat smaller
predators are remnant behavioursfrom a more turbulent past.
The only canid to go extinct in the North Americanend
Pleistocene was the Dire Wolf, C. dirus. The Greywolf, Coyote, and
several foxes survived. In additionto the Dire Wolf, two bears and
three cats wentextinct, all of which were very large (Fig. 2.10).
Canwe learn something about the causes of currentpredator declines
by examining the winners andlosers in the late Pleistocene?
Examination of the
Ancestry 51
much intraguild predation because the victim oftenis not eaten (
Johnson et al. 1996; Palomares and Caro1999; Van Valkenburgh 2001).
Larger carnivores tendto dominate smaller ones and so selection
shouldfavour the evolution of large body size. Large bodysize in
turn selects for a highly carnivorous dietbecause of energetic
considerations. As shown byCarbone et al. (1999), almost all extant
carnivoresthat weigh more than 21 kg take prey as large orlarger
than themselves. Using an energetic model,they demonstrated that
large body size brings with itconstraints on foraging time and
energetic return.Large carnivores cannot sustain themselves on
rela-tively small prey because they would expend moreenergy in
hunting than they would acquire. By tak-ing prey as large or larger
than themselves, theyachieve a greater return for a given foraging
bout.Killing and consuming large prey is best done with
ahypercarnivorous dentition and so the evolutionof large body size
and hypercarnivory are linked. Ofcourse, this does not preclude the
evolution ofhypercarnivory at sizes less than 21 kg, but it
seemsrelatively rare. It has occurred in the Canidae as evi-denced
by the hesperocyonines and the extant ArcticFox, V. lagopus, and
Kit Fox, V. macrotis. However, thetwo extant foxes do not have
trenchant-heeledcarnassials despite their tendency towards a
highlycarnivorous diet, and this may reflect regular,
oppor-tunistic consumption of fruits and invertebrates(Van
Valkenburgh and Koepfli 1993).
Returning to the questions of when and whyhypercarnivory evolves
among canids, it seems thatwhen and why are intertwined. That is,
because ofintraguild competition and predation, selectionfavours
the evolution of larger size in canids and asa consequence,
hypercarnivory. However, when thisoccurs it is largely a function
of other members of thepredator guild. In the case of the
Hesperocyoninae,it occurred relatively early in their history
becausepreviously dominant large hypercarnivores were indecline or
already extinct. In the case of the Boroph-aginae and Caninae, it
did not occur until much laterbecause other clades held the large
hypercarnivorousroles for much of the Miocene. In all these
examples,it appears as though the rise of large
hypercarnivorouscanids reflects opportunistic replacement rather
thancompetitive displacement of formerly dominant taxa(Van
Valkenburgh 1999).
Zubir-02.qxd 20#12#03 7:30 PM Page 51
-
loser species reveals that they tended to be the morespecialized
members of their clades; they were larger(Fig. 2.10) and tended to
be more dentally special-ized for hypercarnivory (Van Valkenburgh
andHertel 1998). Remarkably, two of the species thatwent extinct,
the Dire Wolf and Sabertooth Cat(Smilodon fatalis), are five times
more common in theRancho La Brea tar pit deposits than the next
mostcommon carnivore, the Coyote (C. latrans). This sug-gests that
the Dire Wolf and Sabertooth Cat weredominant predators at this
time, comparable to thenumerically dominant African Lion and
Spottedhyena of extant African ecosystems. The extinctionof the
apparently successful Dire Wolf and Sabertooth
Cat implies there was a major perturbation to theecosystem in
the late Pleistocene. Their demise andthat of the other large
hypercarnivores suggest thatlarge prey biomass dropped to extremely
low levels.Supporting this are the parallel extinctions of 10 of
the 27 species of raptors and vultures (VanValkenburgh and Hertel
1998).
In the late Pleistocene, the largest meat-eaters,both avian and
mammalian, were the most vulnera-ble. Is this the case today for
canids? Of the threelarge hypercarnivorous canids, the dhole, Grey
wolf,and African hunting dog, only the hunting dog ishighly
endangered. Among living canids in general,species that appear to
be most at risk tend to be insu-lar (Darwins Fox, Channel Islands
Fox) or restrictedto limited habitats (Ethiopian Wolf), or just
verypoorly known species (e.g. Short-eared Zorro, bushdog). Indeed,
it is a bit difficult to answer the questionof which of the living
species are most endangeredbecause we have so little information on
many of thesmaller taxa. Nevertheless, it does seem that the
endPleistocene extinction is not a good analogue for whatis
happening at present, at least in terms of which ismost vulnerable.
Then, it was the largest, most abun-dant, and most carnivorous. Now
it seems more oftento be smaller mesocarnivores that are at risk
due tosmall population size exacerbated by habitat loss. Inboth the
end-Pleistocene and at present, the hand ofhumanity looms large as
a cause of predator declines.Initially, the damage was largely due
to overhuntingof both prey and predator, and to this we have
addedsignificant habitat loss. Survivors of the current crisisare
likely to be both dietary and habitat generalists,such as the
Coyote.
AcknowledgementsWe thank David Macdonald and Claudio Sillero
forthe invitation to write this contribution and DavidMacdonald for
his critical review. This research isfunded in part by grants from
the National ScienceFoundation (DEB 9420004; 9707555).
52 Biology and conservation of wild canids
0
100
200
300
400
Vulpes vulpesProcyon lotor
Lynx canadensisLynx rufus
Felis pardalisTaxidea taxusCanis latransCuon alpinus
Gulo guloMiracinonyx trumani
Canis lupusCanis dirus
Puma concolorPanthera onca
Arctodus pristinusTremarctos floridanus
Ursus americanusHomotherium serum
Smilodon fatalisArctodus simus
Ursus arctosPanthera atrox
Body mass
Figure 2.10 North American Pleistocene carnivoransarranged by
body mass. Black bars represent extant species,and white bars
represent extinct species. Arrow indicates the Grey wolf (Canis
lupus). Data from Van Valkenburgh andHertel (1998).
Zubir-02.qxd 20#12#03 7:30 PM Page 52