Implications of Skull Shape For The Ecology and Conservation Biology of Crocodiles

ImplicationsofSkullShapefortheEcologyand
ConservationBiologyofCrocodiles
Proefschrift
terverkrijgingvan
opgezag eijden,
degraadvanDoctoraandeUniversiteitLeiden,
va erH
volg ties
nRectorMagnificusprof.mr.P.F.vand
ensbesluit oorPromo
teverdedig juni2011
vanhetCollegev
enopdinsdag14
klokke 0uur 15.0
door
Ashl rcy
geborenteNashville,Tennessee
eyPea
in1985
Inlovingmemoryofmygrandfather
JosephBoydHurleyIII
January9,1928August28,2008
ii
Chapter1
Linking Conservation and Skull Morphology in the Study of Sympatric Crocodilians:

TheoreticalConsiderations
Abstract
While the idea of linking conservation to morphology is not an entirely new concept, the application to
conservation of sympatric species is a rarely used consideration for skull morphometrics. First,
conservationandmorphologyaredefinedandtheircurrentlinkestablished.Thischapterthendiscusses
the value and methods of integrating skull morphology into conservation of sympatric crocodilians that
will be further explored in this thesis by introducing steps towards integration: analysis of skull
morphometry,interspecificcomparisonofskulls,andintegrationintoaconservationplan.
Conservation
Human development resulted in the possibility to take control over natural environments. Flora and
faunathatposedthreatswereremoved;somewereused.IntheWest,romanticistideasleadtoagradual
shift in the view of nature that included several kinds of previously unconsidered appreciations. With
human development and population increasing, however, wildlife abundance and biodiversity rapidly
decreased.Tocounterthisdeclinewithefficiency,preciseandspecificknowledgeofthewildlifeitselfisa
prerequisitetosuccessfulconservation.
Being the sole reptilian living descendents of Archosaurs (King and Burke 1989) and thus some of the
oldest surviving vertebrates on earth, crocodilians represent flagship species for conservation
movements worldwide. The concept of flagship species means that the public imagination is captured
byonesymbolicspecies,andbyconservingthisspecies,anentirehabitatisprotected.
Thequestforunderstandingthesespeciestakesseveralformsfromthesearchforthelargestcrocodiles,
to how they have survived for so long. Other questions surround behaviour, seeking answers to how
deadly, intelligent, and protective a crocodilian can be. Some of these queries have been answered or at
leastthecuriosityassuagedforthetimebeing.Howbigcanacrocodilegrow?Thelargestextantcrocodile
is the saltwater crocodile Crocodylus porosus which can grow to over six meters (snout to tip of tail)
(Britton 2009). How hard does a crocodile bite? A crocodilian can bite with 9452 N of pressure with
variationdependingonsize(Ericksonetal.2003).Anumberofmorphologicalstudiesexaminingthelast
remainingArchosauriafurtherinvestigatethejawandbody.Scientistshypothesizedhowthesnoutcould
withstandtheforceinvolvedwithtakinglargeprey(McHenryetal.2006).StudiesbyFreyarticulatedthe
physical attributes necessary to sustain erect posture on land (carapace, expaxial musculature and the
vertebral column working in combination; Frey, 1988) and those enabling stronger propulsion through
water (osteoderm connection to tail muscles creating a thoracic bridge; Frey, 1984, 1985), thereby
directly linking the biomechanics of crocodilian movement to its habitat. A kinematic and anatomical
studyhaveevenresolvedthemysteryofthecrocodilegallopbydefiningtheforelimbcharacteristicsand
movement(Meers2003;Renousetal.2002).Despitetheknowledgegained,crocodiliansarestillonthe
endangered species list (IUCN 2010). The most pertinent question remaining is how to preserve self
sustaining,wildpopulations.Whilepreviousresearchersconductedmorphologicalstudiesoncrocodiles
outofcuriosityabouttheorganism,itsabilitytofunctionandsurvive,andevolutionaryandphylogenetic
advancements,afurtherapplicationofmorphologyiswithinconservation.
Whatismorphology?
Morphology is the study of the form and size of an organism or object and its component parts
(Encyclopedia Britannica 2010), or more simply the study of shape. It is sometimes synonymous with
anatomy, although historically the latter refers more to the dissection of bodies by the medical
profession. While morphology is sometimes viewed as an antiquated branch of life sciences, due to
advancements in the fields of genetics and convergent evolution, it is still practiced and advanced
especially with concern to phylogenetics, comparative anatomy and examination of the fossil record.
Morphometrics enables one to define complex shapes in a rigorous fashion and allows for the use of
numericaldataasmeansofshowingrelationshipsordifferences(Webster2006).
1
1
Withinmorphologytherearetwodistinctbranches.First,geometricmorphometricsisthestudyofshape
andonlyincludesdatafromthephysicalspecimen.Statisticalanalysesarebasedonlandmark,outlineor
other similar analyses. Second, functional morphology relates a function of the organism to the shape it
forms, e.g. crocodile snouts in relation to feeding behaviour (Busbey 1995). One can also make
assumptionsofevolutionarygiveandtakeforperformance(Smitsetal.1995).Moprhologyisoneofthe
keyparametersofananimalsphenotype,andthereforeofitsinteractionwithitsenvironment.Theseare
allparatmetersthataresubjecttonaturalselection.
Howcanmorphologybeusedinconservation?
The conservation ofseveral species relies at least in part onmorphological studies. The identificationof
individuals or populations through morphology in order to determine population size, movement and
distribution (Perrin et al. 1991; Whitehead 1990) along with habitat species richness (Edinger and Risk
2000) better focuses conservation efforts. The phylogenetic distinctions provided by morphological
studies led to debates on conservation issues for several endangered species, either increasing or
decreasing the level of concern, such as with marmots (Cardini and OHiggins 2004), spinner dolphins
(Perrin et al. 1991), buckmoths (Rubinoff and Sperling 2004), and dwarf crocodiles (Eaton et al. 2009).
Through the use of morphology, the identification of several new species or subspecies was also
determined, at least in part, by the morphology of those species. With the identification of new species
comes the need for reducing illegal trade or slaughter of endangered populations and redirection of
conservationaction(PrezFarreraetal.2001;Eatonetal.2009).
Howcanmorphologybehelpfultocrocodiles?
Crocodilian husbandry, taxonomy, and evolution all rely, at least in part, on morphological studies.
Researchers used them to determine such critical parameters as growth rates, (Hall and Portier 1994;
Chentanezetal.1983),tosupportphylogeneticstudies(Brochu2001)and,incombinationwithcurrent
genetic studies, to support various hypotheses of taxonomic relationship (Eaton et al. 2009; Willis et al.
2007). These types of studies therefore provide crucial data that underpin evidencebased conservation
initiatives.
Aparticularlyimportantapplicationofcrocodilianmorphologytoconservationconcernsthecoexistence
of apex predators in a shared habitat. Despite knowledge that sympatry in crocodilians is limited and
alreadydividedbytheirecology(Magnusson1985;Herron1994;Ouboter1996;Ross2004),whenmore
than asinglespecies inhabitsanarea,they inevitably have an affecton eachother, especially ifaction is
takenwithonespeciesdisregardingotherspresent(Ouboter1996).Webbetal.(1983)brieflynotedthis
difficulty when a population of C. porosus underwent conservation management causing a population
shiftinthedisregardedpopulationofC.johnsoni(thesmaller,freshwatercrocodile)innorthernAustralia.
They foundanegative correlation between size oftheC. porosus and C. johnsonipopulation (Webb et al.
1983).Thissituationbegstheattentionofconservationistsandawayofdirectingtheireffortswouldbe
through the application of skull morphology to the relationship between the coexisting interspecific
species.
Crocodilianskullmorphometricsinthisthesis
A)Analysisofskullmorphometry
The crocodilian skull has been studied intensely for more than a hundred years (see Mook 1921; Klin
1933). Scientists used it to describe evolution both in the sense of ecology and lineage (Brochu 2001;
SadleirandMakovicky2008).Theallometry,whichistheproportionalgrowthofbodyparts,oftheskull
to the body is a discussion of size (Whitaker and Whitaker 2008) and growth in captive versus wild
populationsasindicatorsofhealth(Coulsonetal.1973;JoanenandMcNease1974).Theskullcontinues
to offer new insights in all fields including coexistence (Pierce et al. 2008). In this thesis, Chapter 2
discusses methods by which to further investigate the skull and Chapter 3 further examines the
2
crocodilianskullusinggeometricmorphometrictechniques.
One issue for which no evidence is available, is the role of the skull in segregating the niche among
sympatricspecies.Whenattemptingtoapplymorphologicalconceptstoecologicalcharacteristics,certain
assumptions must be made. The first assumption is that skull shape is indicative of resources use. A
commonexampleofsnoutshapereflectingresourceuseandevennichesegregationisbillshapeinbirds
2
(Schoener 1965; Smith 1990). While research proves that species with differing skull shapes tend to
inhabit the same areas, the relationship rarely goes further than this (Pierce et al. 2008). The idea of
similar skull shape being indicative of higher competition is a long accepted, but never quantitatively
proven,hypothesisincrocodilians.
For comparative studies of this nature, both the similarities and differences need to be accounted for
within the measurements. Interspecific differentiation must be identified for defining species, while
similarities must be defined to explain ecological competition. Because such studies require a large
number of specimens to assess these characteristics, museum collections are often used for these
purposes.
Five natural history museums were visited: Amsterdam Zoological Museum, Royal Belgian Institute of
Natural Sciences, Senckenberg Natural History Museum, Musum national d'Histoire naturelle de Paris,
and Naturalis Museum, Leiden, The Netherlands to examine skulls for this analysis. The choice was
selective, based on the physical state of the skull. Skulls which were misshapen, through captive
development, having obvious signs of vitamin deficiency such as tooth misdirection or flattened skulls,
were excluded from the analysis. Despite a number of malformed skulls, a large dataset was gathered
(N=159)representingthetwentythreespeciesofcrocodilians.Theseskullswerephotographed(Chapter
r 2)andhandmeasuredforve ificationofphotographicanalysis(discussedinChapter3).
To further supplement the data collected in the museums, information was used from a crocodile
expedition to central Africa, conducted by students from the University of Pretoria. This included body
and skull measurements from African dwarf crocodiles Osteolaemus tetraspis. I also gathered similar
information at Davao Crocodile Park in Davao Mindanao on captive Crocodylus porosus and Crocodylus
mindorensis.
B)Interspecificcomparisonofskulls
Ifitistruethatskullshapeisindicativeofnicheuse,thenasecondassumptioncanbeinferred:similar
skullshapesincoexistingspecieswouldpredicthighercompetition.Researchersalsoexploredthisissue
within other species including birds (Smith 1990), salamanders (Adams 2004), and bats (Aguirre et al.
2002)tonamejustafew.
There are an estimated 31 pairs of sympatric species of crocodilians inhabiting five continents (Figure
1.1), and their relationships become important when executing conservation or management plans
(Ouboter1996;Thorbjarnarsonetal.2006).Whencomparingskulls,inferencescanbemadewithregard
to ecology and niche segregation (Pierce et al. 2008, Pierce et al. 2009). Previous skull comparisons
prove that crocodiles with different snout morphology coexist (Brochu 2001; Pierce et al. 2008).
Thorbjarnarson(1996)suggeststhatsnoutshapeshouldreflectnestinghabitsaswell.Therefore,when
ecology integrates morphology, directional considerations for conservation of limited resources can be
ascertained.
In Chapter 4, I present a comparative study using skull shape to determine estimated population ratios
betweensympatricpopulationwhichwouldreduceinterspecificcompetition.Chapter5furthersupports
the use of head shape as an indicator of realized niche by linking functional physical characteristics to
skullshapethroughallometricrelationships.
3
3
opyright2008byTheNatureConservancyandWorldWildlifeFund,Inc.AllRightsReserved
Figure1.1Mapofcrocodilespeciesrichnessworldwide(WWF/TNC2008)
C)Integrationofresultsintoaconservationplan
Onceacomparisondefinesarelationshipbetweensympatriccrocodilians,theresultsmaybeapplicable.
Conservation plans for areas inhabited by multiple crocodile species must be informed by these
relationships(Thorbjarnarsonetal.2006)becauseapexpredatorpopulations,whenaltered,willinvoke
aresponsefromtheirenvironmentandfromotherapexpredators(Terborghetal.1999).
Integration into a conservation plan would be more effective if focused on reducing the influence of the
limiting factor (Leopold 1933). Habitat is the number one limiting factor impeding success of wild and
reintroduced populations of crocodiles (Ross 1998; Thorbjarnarson 1999), and the connection between
habitat type and population ecology gives insight for conservation and management (Thorbjarnarson et
al. 2006). With habitat loss being such a prime culprit for population failure, interplay between skull
morphometricsandhabitatconservationshouldbeinvestigated.
Intheory,linkingmorphologicalcharacteristicstosympatricspeciesrelationshipswouldbebeneficialto
conservation measures, as it has been to taxonomic studies and husbandry. Despite their ancient
intrigue, crocodilians remain endangered. If we would like to achieve healthy, sustainable populations,
methods for betterdirected conservation plans are a priority. Chapter 6 defines an equation for
determining habitat use by individuals and discusses the intricacies of sympatric species conservation.
Chapter7integratestheequationwiththeanalysisfromChapter4topresentanexamplethroughwhich
skullshapecanbeusedtoenhanceconservationdirectives.
Thisthesisexplorestheconceptthatrelationshipsofcrocodilescanbedefinedbytheirmorphology.The
relationships can be used to determine interaction and to focus conservation efforts in areas where
multiplespeciesexist.
Research Question: Can skull morphology be used as an indicator for conservation methods in areas
inhabitedbymultiplespeciesofcrocodilians?
4
4
Studyobjectives
ns 1.Explorenewmorphometricmethodsasappliedtocrocodilia
2.Defineinteractionrelationshipsbasedonskullmorphology
3.Demonstratetheapplicationofrelationshipsfromskullshapetoconservationmethods
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Analysisofskullmorphometry
Youngcat,ifyoukeepyoureyesopenenough,oh,thestuffyouwouldlearn!Themostwonder fulstuff!
Dr.Seuss
8
8
Chapter2
SuggestionsonPhotographingCrocodileSkullsforScientificPurposes
+
Abstract
Herewedescribemethodsforphotographingcrocodileskulls.Thequalityofthesephotographswasthat
necessarytosuccessfullycompletedigitalphotographicanalysis.Weofferthismethodasaguidelinefor
standardizing methods for photographing crocodile skulls or at least as an example of how indepth a
description of methods should be in order that other scientists may compare data and account for
differences in methods. We also present the accessibility and effectiveness of using a digital camera as
meansofdatacollection.
Introduction
In cranial morphometrics, an effective way of obtaining data for analyses is by using photographs or
drawings.Withanaveragedigitalcamera,computerandsoftware,itisnowpossibletoextractextensive
informationonsize,shape,location,surfacearea,andcolor.Existingphotographsordrawings,however,
may not always be suitable for metric comparisons because of optical distortion, light conditions, used
background, or inconsistency in type and position of the camera or skull (Frie 2003). Ideally an
applicable standardized method would be used in all photodocumentation and photoresearch. For
practicalpurposeshowever,aproperandcompletedocumentationofexactmethodsusedwouldsuffice.
to nvert Itwouldallowotherauthors usetheinformationorco theacquireddatatomatchtheirown.
We describe and discuss a method used successfully in morphological research on crocodile skulls
(Chapter 3 & 4) with regard to applicability and effectiveness. We also discuss object orientation with
respecttothecamera,opticaldistortion,andallmaterialsused.
Generalsetupandmateri
We placed the skulls on a floor using a black towel as background. We used a Panasonic Lumix DMC-
FX107 digital camera set to intelligent AUTO mode, 3072 by 2304 pixels, J PEG/
als
Exif format. We positioned the
camera, mounted to an adjustable aluminum tripod placed on the floor positioned directly over the skull. For
each picture, we set the camera to automatic-mode, with a two-second timer to prevent movement blur from
pressing the shutter button, the lens range was 28mm - 102mm and aperture range F2.8 - F5.6. The grid in
ns display options enabled a non-essential, but convenient way of lining up specime within the field of view.
We inverted the center column of the tripod together with its head, thus centering the camera on the
saddle plate between the legs of the tripod, directly perpendicular to and facing the skull. Because
crocodileskullshaveawiderangeofheight,distancefromspecimenshadtoarbitrarilyvaryfrom40cm
120cmforconvenience.Weusedamixtureofflash,daylightandambientlight.
We leveled specimens using a spirit level. In all cases, the aim was to bring the surface bones
photographed and the plane of the photograph into a parallel relationship, thereby equalizing and
inimizingparallaxdistortioninalldirectionsawayfromthefocalpoint. m
+
Pearcy,A.andZ.Wijtten(2010)Suggestionsonphotographingcrocodileskullsforscientificpurpose.
HerpetologicalReview41(4):445447
9
Orientationofsubjectandcamera
Dorsalviewofcranium
Figure 2.1 showsthedorsalviewofthecranium.Thereddotshowsthecenter point along the midline of the skull

andthefocuspointofthecamera.
This view is most commonly used for comparative studies between crocodilian species (Figure 2.1).
Preferably cranium only was used so that the skull rested on the pterygoid flanges evenly; where these
were uneven, we leveled the skull widthwise along the cranial table. If cranium and jaw could not be
detached,thesamelevelingtechniqueswereused,andthelowerjawdisregardedforanalysis.Weraised
thesnoutwithpaddingtobringthetopofthepremaxillarynaresapproximatelyleveltotheplaneofthe
cranial table and parallel to the plane of the floor. The camera focal point (red dot) was at the center of
themidline.
Ventralviewofcranium
Figure2.2showstheventralviewofthecrocodilianskull.
In the ventral view of the cranium, the cranium rests on the cranial table, and we elevated the anterior
endofthesnouttobringthesnout,palateandmaxillarytoothrowlevelparalleltotheplaneofthefloor
(Figure2.2).Thecamerafocalpointwasatthecenterofthemidline.
Occipitalview
(a) (b)
\Figure2.3(ab)showstheoccipitalviewofthecranium(a)andthelevelingoftheskullforthefocuspoint(b).
Theoccipitalview(Figure2.3a)isnotcommonlyrecorded.Wepositionedtheskullwithmandiblesinthe
samemannerasforthedorsalview,withthesnoutraisedtobringthetopofthenaresandtheplaneof
thecranialtableapproximatelylevelandparalleltotheplaneofthefloor(Figure2.3b).Thecamerafocal
pointfrombehind(posterior)isthetipoftheoccipitalcondyle.
10
10
Lateralviewcranium
(a)
(b)
Figure2.4(ab)showsthelateralviewoftheskull(a)andtheaimofthecamera(b).
Theskullrestsnaturallyonitsmandibularrami,withthecameracenteredlaterally(Figure2.4a).Inthis
way,wecancomparethesnoutandposteriorportionoftheskull.Thefocuspointishalfwaybetweenthe
tipofsnoutandthearticularextensionofthejaw(Figure2.4b).
Lowerjawdorsalview
Figure2.5showsthelowerjawsofthecrocodileskulls.Whilethisdiagramisfromthedorsalview,ventralviewis
donesimilarly.
Researcherscanusethisviewforstudyingthemandibularsymphysisandotherbasicjawcomponents.
Thejawsitsonthemandibularramiwiththeanteriorendofthejawelevatedtobringthemaxillarytooth
rowlevelandparalleltothefloor(Figure2.5).Fortheventralview,thejawsitsonthearticularsurfaces
iththeanteriorendofthejawelevatedtobringthemaxillarytoothrowlevelandparalleltothefloor.
hefocuspointforbothjawviewsisthecenterofthevirtualmidlinebetweenthemandibles.
w
T
Discussion
In this discussion, we elaborate on the methods used and, where applicable, consider other options and
improvement.Generally,researcherschoosemethodsaccordingtotheintendedmeasurementsofstudy.
We state, however, that in many situations using a general standardized method when photographing
crocodileskullswouldmaximizetheuseofaphotographandthusbepreferable.
Levelingaskull,ingeneral,makesforarepeatablemethod.Liftingtheskullindorsalperspectiveallows
fortheviewoftheanteriorendofthetipofthesnoutinsteadofjustthetopofthepremaxilla.Notleveling
the skull in ventral view, a technique applied often (see Dead Crocs Database), is more convenient and
would show more of the skull; however this does make extracting measurements from pictures nearly
impossible due to depth differences. Positioning of the skull in occipital view is, as far as we are
concerned, amatter ofchoice. Depth differences are relatively large, thus the view is not normally used.
We chose to level the skull to have a better view of the tip of the vertebral condyle as areference point.
Artificially adapting the position of the skull when resting on a horizontal surface in lateral view would
exposemoreofthelowerjawandlessoftheupper,althoughveryminimally,duetotheflattenedskullof
acrocodile,renderingsuchactionsvirtuallyuseless.Indorsalviewofthelowerjaw,weleveledthejawin
arepeatableway.Apartfromenhancingaccuracyoflaterdistancemeasurements,thisactionalsoexposes
11
anoftenresearchedsubject,theteethandtheirsockets,moreevenly.
Any optical lens leads to distortion of the absolute and relative dimensions of an object like a skull. The
outer edge of the skull will be invisible in a central projection, affecting absolute dimensions.
11
Furthermore,objectsthatareclosertothefocalpointwillappearrelativelylargerthantheyactuallyare,
comparedtoportionsthatarefurtheraway,affectingtheproportionsoftheobject.Inpracticality,taking
a picture of a cranium with a distance of one meter results in a distortion of a maximum of 7.5%
(Jacobshagenetal.1988)andsocalledbarrelorpincushiondistortionisnegligibleusingnonspecialist
lenses.Mostdistortionscanbeavoidedbystereophotographictechniques.Anotheroftenusedtechnique
is resorting to reference objects a ruler for instance so that the sizes can be calibrated. We believe,
however,thatintheinterestofapplicability,increasingthedistancebetweenthecameraandtheobject,
which significantly reduces the photographic error, or resorting to mathematical solutions like a
Generalized Procrustes Analysis (Rohlf 1999; Bookstein 1996) as we did, are more preferable solutions.
Inmanysituations,adaptingonesmethodstorenderopticalerrorminimalisthebestsolution.
Backgrounds,formostpurposes,mustbeincontrasttothesubjectasmuchaspossible.Forthegenerally
whiteskulls,weusedablacktowel.Contrastdecreasesambiguitybetweentheskullandbackground,and
darker backgrounds will reduce the amount of artifacts caused by shadows or reflection. Both lead to
more precise definition. However, in some situations, it might be worth considering using a background
color that is unlikely to be present in the subject, as software would then be able to filter this color
independentofthesubjectcolor.
Photographersprefermultidirectionallightinginordertobetterdefinetheedgesoftheobject.However,
withablackbackgroundandabrightflash,especiallysoneartotheobject,edgedistortionduetolackof
light,inthismethod,isminimal.
With the accuracyof distance measurements roughly increasing with the square root of the pixel depth,
weconsidera7Megapixelcamera,givinganestimatederrorof0.05cmonan80cmspecimenaboutthe
minimum for most applications with crocodile skulls. The tripod may not always be a necessity. It does,
however,lendstabilizationtothecamera,especiallyimportantinselftimedshots.
Not all studies have the funding to use stereographic techniques or do CTscans, which would reduce
distortioncompletely,andwouldallowforacomprehensiveassessmentofmeasurements.Themethods
presented here are costeffective, while reducing distortion. Museums and conservation groups can
follow these methods for their databases in order to have a comparable method, repeatable by anyone
with a digital camera and material for a background. If not applied, at least the presented description
should serve as an example to the extent required to allow other researchers to convert their data into
comparablematerial.
Acknowledgements Mr. Franklin Ross for input and advice. Amsterdam Zoological Museum, Royal
Belgian Institute ofNatural Sciences, Senckenberg Natural HistoryMuseum, Musum national d'Histoire
naturelledeParis,andNaturalisMuseum,Leiden,TheNetherlandsforaccesstotheircollections.
References:
Bookstein FL (1996) Combining the tools of geometric morphometrics. In LF Marcus, M Corti, A
Loy, G Naylor and D Slice (Eds) Advances in Morphometrics. Plenum Press, New York, pp 131-
151

DeadCrocsDatabase.Viewed20September2010<http://www.bsc.ufl.edu/staff/kvliet/deadcrocs>
FrieM (2003) An application of the relative warps analysis to problems in human paleontology with
notesonrawdataquality.ImageAnalysisandStereology2003:22:6372
JacobshagenB,BerghausG,KnumanR,SperwienA,ZeltnerH(1988)FotogrammetrischeMethoden.In:
numann R, ed. Anthropologie. Handbuch der vergleichenden Biologie des Menschen. Band I, 1.Teil. K
Stuttgart:Springer,32845
RohlfFJ(1999)Shapestatistics:Procrustessuperimpositionsandtangentspaces.JournalofClassification
6(2):197223 1
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12
Chapter3
ALandmarkAnalysisofCrocodilianSkulls
+
Abstract
Thispapertacklesthecomplicatedproblemofskullmorphometricsinseparatingspeciesofcrocodilians.
It presents new perspectives on the variety and variability in skull shapes of crocodiles using both
traditional and nontraditional measurements within a landmark analysis. I found that total width and
length do not account for the most variation between crocodilian species and suggest using
measurements between the orbit and premaxillary notch, orbit to 5
th
maxillary tooth and also Klins
number12(1933)asareasofvariabilitybetweenspecies.
Introduction
Grouping and taxonomy of animals is a large part of zoological studies, and a constant debate among
scientistswhostudyCrocodylia(Norell1989,Brochu2000).Theshapeoftheskullisthemostsignificant
distinguishing feature of different crocodilian species. Apart from being useful in species division, head
shape is relevant to fields of crocodile ecology, behavior, evolution and conservation (Ouboter 1996;
Brochu 2001a; McHenry et al. 2005; Sadleir and Makovicky 2008). To date, the most variable aspects
within documented skull morphology of extant species are maximum length and width (Pierce et al.
2008). This current description of skull shape is limited and group descriptions are nowhere near
ersityinskullshapewithinc sufficienttoaccountforthediv rocodilians(Pierceetal.2008).
Scientists previously grouped crocodilians into two categories based on their rostral shapes, namely:
longirostrine and brevirostrine (Busbey 1995) (long and shortsnouted, respectively). While these
groups were reflective of obvious physical characteristics within the snout, further research illustrated
these to be insufficient for describing the variety of rostral shapes within Crocodylia. In 1995, Busbey
(1995) further divided crocodilian snouts based both on length and width, as previously done, and on
lateral profile (platyrostral and oreinirostral). Despite the categories being useful for descriptions,
Busbey stated that they are not taxonomically definitive, due to overlap in head shape between similar
taxa. In 2001(a), Brochu added to the groupings of Busbey to include ziphodonts (deep, laterally
compressed snouts) and duckfaced, based on the inclusion of fossil specimens within Archosauria. He
alsosuggestedminorchangeswithintheexistinggroupsofBusbey.Brochuconcludedthattheskullwas
phylogenetically plastic and that similar snout shapes had arisen several times in disparate lineages
(2001a). In 2003, another study (Marugn-Lobn and Buscalioni 2003) suggested a return to three skull
types(meso,longi,andbrevirostral)basedonlateralviews,ratherthandorsalviews,usingpercentages
of brain case vs. orbit vs. rostrum. Other studies define evolutionary correlation of skull shape between
differentrostralshapegroups(SadleirandMakovicky2008).Thischapterwillprovidevaluableinsights
intospeciesidentifyingskullcharacteristics.
The aimof this chapter is to give more detailed insightintothe varietyand variability of skull shapesof
crocodiles.Webaseourstudyonmorphometricparametersusingconsistentfeatures,landmarks,clearly
presentinthewholeorderthatreflecthomologouspointsontheskull.Webelievethechosenpointsare
of both ecological and evolutionary significance, and include parameters of both traditional and
nontraditionalmeasurements.
Methods
We collected data on 159 adult crania of all 23 crocodilian species from five European museums
(AmsterdamZoologicalMuseum,RoyalBelgianInstituteofNaturalSciences,SenckenbergNaturalHistory
Museum, Musum national d'Histoire naturelle de Paris, and Naturalis Museum, Leiden, The
Netherlands). We photographed the skulls in dorsal view for twodimensional digital analysis. Placing
eachonablackcloth,weleveledthemalongthemedialsuturefromthehighestpointonthecranialtable
tothehighestpointattheanteriorendofthesnout,exposingmoreoftheskullsurfaceinamoreuniform
fashion.Wepreferredcraniumonlysothattheskullrestedonthepterygoidflangesevenly;wherethese
were l widthwise along the cranial table. If cranium and jaw could not be
det ngtechniques,disregardingthelowerjawforanalysis.
uneven, we leveled the skul

ached,weusedthesameleveli
14
+
Pearcy,A.andZ.Wijtten(inrevision)Amorphometricanalysisofcrocodilianskullshapes.HerpetologicalJournal
13
We photographed dorsal views of specimens using a Panasonic Lumix DMCFX107 digital camera set to
intelligent AUTO mode, 3072 by 2304 pixels, JPEG/Exif format. We set the camera perpendicular tothe
center of the cranium along the midline axis using a tripod at a minimum distance of 40cm and a
maximumdistance of 120cm from the specimen based on thesize of thespecimen in orderto keep it in
the field of view. To light the skull, we used flash, natural light and ambient light against a black
background. We plotted landmarks on the crania (Figure 3.1, Table 3.1) using the digital images in the
programImageJ(Rasband2009).
Wechoselandmarksatlocationsrepresentingtraditionalmeasurementssuchastipofsnout(anteriortip
of premaxilla)(1), medial, posterior edge of parietal bone (15) and widest point on the cranium (13,14)
andatareas,whichhaveanobviousphysicalcharacteristic(Figure3.1,Table3.1).Weincludedtheseas
landmarksastheyaccountfortraditionalsizemeasurementsoftotallengthandtotalwidth.Landmarks
49 are locatable, obvious points within a dorsal view of a cranium. Landmarks 4 and 5 are often
associated withthe 5
th
maxillary tooth, while landmarks 6 and 7associate withthe 6
th
maxillary. This is
variable between species. Landmarks 47 can be difficult to locate on longirostrine groups such as
Gavialis and Tomistoma; however, they are apparent in most other species. Finally, we also adopted a
usefulmeasureofskullwidthdescribedbyKlin(1933)consistingofthewidthoftheskullmeasuredat
the anterior point of the postorbital bar suture (Klin 12). We present Klin 1212 (1012) here as we
alsosuggesteditasalocationformeasuringsizewithinCrocodylia(Appendix3).
For comparative purposes,validatingthe use of landmarkanalysis in this study, we took measurements
usingacaliperfortotallength,totalwidth,widthatKlin1212andlengthfrommidlineofKlin1212to
theanteriortipofthepremaxillaecontact(tipofthesnout)alongthelongaxis.
DataAnalysis
We used a General Procrustes Analysis (GPA) to standardize the coordinate data, removing unwanted
effectsofsizeandrotation.Fromthestandardizeddataresiduals,weranaprincipalcomponentanalysis
(PCA) to determine the amount of variability accounted for by each landmark. The first PCA considered
all landmarks, the second removed highly variable landmarks, and the third explored a noted area of
variation. We used a cluster analysis with the same data to examine division between species. We used
PAST:PaleontologicalStatisticsSoftware(Hammeret.al2001)toconductallanalyses.
Using coordinates of each landmark extracted form the digital pictures, we calculated the distances for
total length, total width, width at Klin 1212, and length from Klin 1212 along the to the tip of the
snout. Using PAST (Hammer et al. 2001), we conducted a Pearson correlation between these
measurementsandthesamemeasurementstakenwithacaliper.
Table3.1Locationofusedlandmarkswithincrocodilianskull
Landmark PointLocation
1 Anteriortipofpremaxillaecontact
2 Minimumwidthimmediatelyposteriortopremaxillamaxillacontact(notch),leftside
rightside 3 Minimumwidthimmediatelyposteriortopremaxillamaxillacontact(notch),
4 Maximumpreorbitalwidthposteriortopremaxillamaxillacontact,leftside
5 Maximumpreorbitalwidthposteriortopremaxillamaxillacontact,rightside
lwidthposteriortomaximumpreorbitalwidth,leftside
widthposteriortomaximumpreorbitalwidth,rightside
6 Minimumpreoribita
7 Minimumpreoribital
t 8 Centerofleftorbi
9 Centerofrightorbit
10 Klin12leftside
11 MidlineatKlin12
12 Klin12rightside
13
14
15
Maximumwidthquadratojugalbone,leftside
Maximumwidthquadratojugalbone,rightside
Posteriortipofsupraoccipital(medialposteriormarginofcranialtable)
15
14
16
Results
Pearson correlations between the ratios of 1314:115 (cranial width to total skull length) determined
Figure3.1GeneralpositionoflandmarksoncraniumcorrespondingtoTable3.1(dorsalview)
usingbothdigitalandcalipermeasurementmethodswere0.908(p>0.01,o=0.01).
Aninitiallandmarkanalysisevaluated15landmarksinaPCA.Thefirstthreecomponentsexplainedthe
majority of the variance (81.6%), with PC 1 accounting for 68.1%. When reviewing case loadings, we
found that landmarks representing the premaxillarymaxillary (pm) notch and the landmarks 47,
associatedwithpreorbitalminimumandmaximumwidths,drivePC1.Wederivedthefirstindicationon
the ability of our data to distinguish species by performing a hierarchal cluster analysis (correlation
coefficient=0.7734).Sincethetestshowedsomesuccessfuldivision,itlegitimizedfurtheranalysisofthe
data.
Figure3.2showsthatPC1anditsdrivingforcesalignedwithrelativerostralength.Allspeciestothefar
right expressed a longirostrine phenotype. G. gangeticus and T. schlegelii were at the outer limits of the
grouping. However, species to the left of the PC1 axis overlapped and represented all other variations
fromtheextremebrevirostrineA.mississippiensistothewidevarietyofCrocodylussnouts,excludingthe
xtremelongirostrines(C.cataphractusandC.johnsoni). e
15
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.
1
6
16
WerepeatedthePCA,omittinglandmarks4,5,6and7sincethesearedifficulttolocateonsomespecies.
In this, the first three components at 80.6%, predominantly explain the variance, 62.9% of which is
explained by component 1. When we examined case loadings, the driving factor for the component was
thepmnotch,representedbylandmarks2and3.Landmarks10and12,representingKlin1212,drove
thesecondcomponent(10.2%).Aseparateclusteranalysisshowedacorrelationsimilartotheprevious
analysis(0.7463).
WeusedanotherPCAtoexplorethenotedareaofvariationbetweenlandmarks2,3and8,9(Figure3.3).
Wecalculatedthedistancesbetweenlandmarkstogeneratemultipledistancesbetweentheorbitandthe
pmnotch(97,75,53,73,and95).Principalcomponent1,whichisdrivenbythedistancesbetween
the orbit and maximum preorbital width, explained 90.0% of the variance. When we compared these
landmarks in a cluster analysis, there was notable clustering (correlation coefficient 0.7639) similar to
thepreviousanalyses.
Figure 3.3 mimicked the same gradient of figure 3.2 along rostra shape, with the extremes (C. latirostris
andT.schlegelii)beingpresenttothefarsidesofthecluster.However,therewasaslightdeviationasA.
mississippiensisskullshapeexpressionmovedclosertotheclusterofotherspecies.ThiswasduetoPC2,
seeminglydrivenbyasizegradient,withsmallerspeciesalongthenegativeaxisandsturdieranimalson
hepositiveaxis. t
PCAofdistancesalonglateralmargin
Figure 3.3 PCA comparing all length measurements along lateral margin between the orbit and the premaxillary
notchwithindifferentspecies
18
17
Discussion
This shape study used 159 skulls from all 23 species of crocodiles. Although a landmark analysis is not
fully extensive and only dorsal views were considered, we think it safe to make statements on general
areasofimportancepertainingtovariationinsnoutshape.Wearguethattheareabetweenthepmnotch
andtheorbit,thedistancebetweentheorbitandmaximumpreorbitalwidth,andthewidthoftheskullat
Klin1212eachhaveanobvious,andpreviouslyunattended,significance.
Bybroadeningthescopeandintegratingobviousareasofvariationaroundtheorbitandlateralline,we
foundthatthepreviouslyconsideredtotallengthandwidthmeasurementsarenotthestrongestfactors
affecting variation between species (Pierce et al. 2008; Sadleir and Makovicky 2008). The initial PCA
resonatedwiththishypothesis.Pointsalongthelateralmargin,however,aredifficulttolocateinextreme
longirostrine species such as G. gangeticus and T. schlegelii and might create unwanted artifacts.
Therefore, we further investigated the relevance of our findings by removing landmarks susceptible to
dissimilarityandfoundourhypothesisstrengthened.Sinceskullshapeistheforemostimportantphysical
attributeindistinguishingcrocodilespecies,thisinformationwouldbeusefulincrocodileecomorphology
withrelationtoontogeny,suitabilityofhabitat,andhuntingandfightingtechniques.
Within the region between the pm notchand the orbit, the distance between the center of the orbit and
the maximum preorbital width showed to be an important variable pertaining to the cluster analysis.
Differentlocationswithinthisareaweresubjecttoconsiderationasmarkedvariantsbetweencrocodilian
species. For instance, Hall (1994), Joffe (1967), and Verdade (2000) studied variation in orbit size and
hypothesized it to be linked to several functional ecological factors. Because of interspecific orbit
variation, it is not unlikely that distances from this area to other parts on the skull would vary between
species.Thedistancesbetweentheorbitandotherpartsoftheskullcould,possibly,beusedtodefinethe
relationshipbetweenfeedingbehaviorandprotectionoftheeyeorambushtechniques.
By broadening the scope, integrating less obvious areas such as Klin 1212, we were able to assign
Klin1212 within both PCAs as a driving force of variation between species. This driving force may
justify its selection as a constant measurement for size (Appendix 3). The absence of driving force of
similartraditionallengthandwidthmeasurementsstrengthensthishypothesis.
Pertaining to the division of species, we could state that the three skulltype morphology system of
MarugnLobn and Buscalioni (2003) might be helped by inclusion of pm notch to orbital shape
characteristics. An interesting application is also the possible strengthening of Brochus (2001a)
hypothesis of phylogenetic plasticity when considering the wide variation of orbital to pm notch snout
shapeindisparatearchosaurlineages(Brochu2001b).
Conclusion
In this study, we showed that traditional measurements of total width and total length of the skull may
not be the best speciesspecific indicators. The results indicated the presence of a stronger identifiable
variance between species when we considered Klin 1212 and maxillary length measurements. We
identifiedtheorbitaltopmnotcharea,Klin1212,andthedistancebetweenthecenteroftheorbitand
the maximum preorbital width as main focus areas for species differentiation. The measurements
analysed usefully define the shape of the crocodilian skull, differentiate between species with good
precision,andallowreasonableinferencesaboutfunction.Inthismanner,thesemeasurementswouldbe
avaluableintegrationintointerspecific,comparativemorphologystudieswithinCrocodylia,investigating
ecologyandevolution.
Acknowledgements
Dr.FransWitteandDr.MasonMeersfortheircommentstothemanuscript.FranklinD.Rossforadvice
on measurements. Amsterdam Zoological Museum, Royal Belgian Institute of Natural Sciences,
Senckenberg Natural History Museum, Musum national d'Histoire naturelle de Paris, and Naturalis
Museum,Leiden,TheNetherlandsforaccesstocrocodilianskullcollections.
19
18
References:
BrochuCA(2000)PhylogeneticrelationshipsanddivergencetimingofCrocodylusbasedonmorphology
andthefossilrecord.Copeia2000(3):657673
BrochuCA(2001a)Crocodyliansnoutsinspaceandtime:phylogeneticapproachestowardsadaptive
radiation.AmericanZoologist41:564585
BrochuCA(2001b)Progressandfuturedirectionsinarchosaurphylogenetics.JournalofPaleontology
75:11851201
Busbey III A (1995) The structural consequences of skull flattening in crocodilians. In J Thomason (Ed):
Cambridge,pp173192 FunctionalMorphologyinVertebratePaleontology.CambridgeUniversityPress,
Hall PM, Portier KM (1994) Cranial morphometry of New Guinea crocodiles (Crocodylus novaeguineae):
ontogeneticvariationinrelativegrowthoftheskullandanassessmentofitsutilityasapredictorofsex
andsizeinindividuals.HerpetologicalMonographs8:203225
Hammer,HarperDAT,RyanPD(2001)PAST:PaleontologicalStatisticsSoftwarePackageforEducation
andDataAnalysis.PaleontologicalElectronica4(1):9pp.http://palaeoelectronica.org/2001_1/past/
issue1_01.htm
Joffe J (1967) The dwarf crocodiles of the Purbeck Formation, Dorset: a reappraisal. Paleontology
9 10:62 639
MarugnLobn J, Buscalioni AD (2003) Disparity and geometry in the skull Archosauria (Reptilia:
Diapsida).BiologicalJournaloftheLinnaeanSociety80(1):6788
McHenry CR, Clausen PD, Daniel WJT, Meers MB, Pendharkar A (2005) Biomechanics of the rostrum in
crocodilians: a comparative analysis of finiteelement modeling. The Anatomical Record Part A 288A:
827849
Norell MA (1989) The higher level relationships of the extant Crocodylia. Journal of Herpetology
23(4):325335
threepredators.SPBAcademicPublishingbv,Amsterdam,theNetherlands
o modelingapproach.JournalofMorph logy269:840864
Rasband WS (19972001) ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA,
http://rsb.info.nih.gov/ij
SadleirRW,MakovickyPJ(2008)Cranialshapeandcorrelatedcharactersincrocodilianevolution.
JournalofEvolutionaryBiology21:15781596

Verdade LM (2000) Regression equations between body and head measurements in the broadsnouted
aiman(Caimanlatirostris).RevistaBrasileiradeBiologia.60(3):469482. c
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Interspecificcomparisonofskulls
Soyousee!There'snoendtothethingsyoumightknow,dependinghowfarbeyondZebrayougo.
Dr.Seuss
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20
Chapter4
Defining Niche Segregation Between Sympatric Crocodilian Species Using Skull
MorphospaceAnalysis
+
Abstract
This study assumes that similarity in morphological characteristics increases competition between two
species. From this assumption, we determined morphospace overlap and used it to estimate ecological
relationship.Ievaluatedsympatricpairsofcrocodilians,ascoapexpredators,andassessedtheinfluence
ofthesemorphologicalfeaturesupontheconservationandmanagementofmultispeciesenvironments.
Introduction
Apex predators tend to prey, but not be preyed upon, in their given food chain. Crocodiles are distinct
apex predators in that separate species, which are extremely similar in shape and size, share a niche
within the same system and divide that niche by specializations in anatomy, physiology and ecology to
coexist (Ouboter 1996). Many of these factors can be related either directly or indirectly to the
morphological characteristics of each species. Researchers focused on the head as the focal point for
defining this proportionality not only as it allometrically increases with body length (Greer 1974;
Woodwardetal.1995),butalsobecauseforspeciescomparison,itisthemostnotablydifferentphysical
attributewithincrocodilians.Inthisstudy,theheadanditsassumedproportionalitybetweenotherparts
of the body, which may affect ecological niche separation, will be used to examine the impact of a
sympatric species on its coinhabitant(s). Working under the assumption that the more similar two
speciesare,themorelikelytheyaretobeincompetition,thispaperusesskullmorphometricstodefine
thelikelihoodofcompetitionbetweensympatricspecies.
Thereareseveralsetsofgeographically(aslistedinOuboter1996)sympatricspeciesofcrocodilians.Of
these, very few would overlap directly in habitat (Ross 2004). However, Pierce et al. (2008) noted that
when a geographically sympatric pair of crocodilians existed, each had a different snout shape (out of
threepossiblevarieties).Thissuggeststhatdifferenceinshapemayreducecompetitionbetweenspecies
allowingforcoexistenceevenonalargergeographicscale.
Consideringgeographicallysympatriccrocodilianspecies,Webbetal.(1983)foundthattheconservation
ormanagementofonespecies(notoftheother)doeshaveaneffectontheuntargetedspecieswithinthe
syntopic zone. As these are large animals and top predators, they would likely have a ripple effect
throughout their environment when it comes to conservation or management practices (Terborgh et al.
1999).Thisrippleisprobablymostevidentincoapexpredatorsascompetitionforresourcesalterswith
eitherpractice.
Thischapterexaminesskullmorphometricsincrocodilianstoassesssympatricrelationships.Wechosea
selectionofgeographicallysympatricspeciesforexaminationinordertodevelopdetailedassessmentof
morphological indicators of sympatry. This information will benefit conservation areas in multispecies
environmentsasitassessesasimplisticformindexofcompetition:morphospaceoverlap.Morphospace
istherepresentationofapossibleform,shapeorstructureofanorganismwhereeachaxeswithinthen
dimensionscorrespondswithacharacteroftheorganism.Wegiveavisualaidshowingbasicskullshape
overlapcomparedwithgeographicaloverlapinAppendix4.
Methods
Wephotographedcrocodilecraniarepresenting23extantspeciesfromfivemuseumsintheirdorsalview
using a Panasonic Lumix DMCFX107 digital camera set to intelligent AUTO mode, 3072 by 2304 pixels,
JPEG/Exif format. To keep the whole specimen in the field of view, we set the camera perpendicular to
the center of the cranium along the midline axis using a tripod at distance. We then placed landmarks
withintheimages(Figure4.1)onthecraniausingImageJ(Rasband2009).WeextractedXycoordinates
for ndmark coordinates through a General Procrustes Analysis to remove
size umbers were then analyzed using a Principal Components Analysis to
each landmark and ran the la
and rotation factors. These n
22
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PearcyA(inreviewJanuary2011)Definingnichesegregationbetweensympatriccrocodilianspeciesusingskull
morphospaceanalysis.Herpetologica
21
acquire information on variation in shape of crania. Snout shapes fell along a gradient from broad to
slendersnouted.Weconsideredtheextremesnoutshapestofilllessnichespaceduetospecializations.
Figure4.1Locationoflandmarksincrocodilianskull
We used the xy coordinates to calculate distances between specific landmarks in number of pixels. We
took a reference measurement from the physical specimen in order to calculate estimated actual
distances from the distance calculated from pixels. We then used the actual distance measurement to
calculatethemorphospaceoverlapfollowingmethodsdescribedinComptonetal.(2007).Wecalculated
the interquartile range and total range for each measurement within each species. As a robust statistic,
we preferred interquartile range to reduce the affect of outliers or abnormal specimens. We compared
each group of sympatric species separately. We calculated both the sum of the interquartile ranges and
thesumofthetotalrangesforeachspecies.Bydividingtheinterquartiletotalbytheoverallrangetotalof
thecomparedspecies(Equation4.1),wecalculatedmorphospaceoverlap.Freespaceisequivalenttothe
morphospace occupied by only one of the sympatric pair of the combined total space occupied by the
sympatricspecies.
Equation4.1Theequationusedtocalculatemorphospaceoverlapbetweensympatricspeciesofcrocodilian
UsingSPSS16.0,wecorrelatedthecrocodilemeasurementsusingaPearsoncorrelation.
Results
We took measurements from a total of 159 specimens representing from 1 to 17 specimens of each
speciesandcoveringasizerangeofsubadulttoadultwithineachspecies(Appendix1).
To reaffirm the value of these measurements as indicators of speciesspecific differentiation and usable
for defining ratios derived from morphospace overlap, we again present results from Chapter 3 with a
visual aid (Figure 4.2). The principal components analysis found that the first three components
explained the majority of variance (81.6%) with PC 1 accounting for 68.1%. Skulls along PC1 varied by
shape and along PC2 by size (Figure 4.2). The shape extremes varied from the broadsnouted Alligator
mississippiensistotheslendersnoutedG.gangeticus.
23
22
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23
Australia
Morphospace overlap between Crocodylus johnsoni and Crocodylus porosus is 0.337. C. porosus (63%)
primarilyfilledthespace,withonly37%beingassociatedwithC.johnsoni(Figure4.3).Thesespeciesare
highlycorrelated(0.932,p=0.01).
Figure 4.3 Pie charts showing the overlap in morphological characteristics and the division of overlap between
AustralianCrocodylusspp.
If assumed morphospace is equivalent to niche space, 34 of 100 crocodiles would overlap within a
syntopic zone. Of these, 21.24 (=0.34 x 0.63) would be C. porosus and 12.58 (= 0.34 x 0.37) would be C.
johnsoni.ForeveryoneC.porosus,0.59(=0.37/0.63)C.johnsoniwouldbesuccessfulatcoexistence.
India
In India, the differing snouts of Crocodylus palustris and G. gangeticus (corr.=0.833, p=0.01) created a
morphospaceoverlapof0.46.ThedivisionfavoredC.palustris(28%)totheslendersnoutedspecialistG.
gangeticus (18%) (Figure 4.4), or for every one C. palustris, 0.67 (=0.40/0.60) G. gangeticus could
successfullycoexist.

Figure4.4Piec artsdisplayingmorphospaceoverlapbetweenG.gangeticusandC.palustris h
SouthAmerica
Seven different species of crocodilians live in different countries and different sympatric groupings
throughout South America(see Ouboter1996). Here, we compared two caimansCaiman crocodilus and
Melanosuchusnigerinmorphologicaloverlap(Figure4.5).
25
24
Figure4.5PiechartsshowingoverlapinskullmorphologyofM.nigerandC.crocodilus
Therewasa50%overlapinmorphologicalcharacteristicsbetweenthetwocaimans.Whenweexamined
the overlap, the morphospace was nearly divided evenly (46% M. niger and 54% C. crocodilus). The
specieshadahighcorrelation(corr.=0.996,p=0.01).
Africa
NativetoAfricanfaunaarethreespeciesofcrocodilian:Crocodyluscataphractus,Crocodylusniloticusand
theAfricandwarfcrocodileOsteolaemustetraspis.Becausethesethreediffermarkedlyinsizeandshape,
the morphospace overlap was only 39%. When further divided by species, C. niloticus took the most
space at 39% followed by O. tetraspis (33%) (Figure 4.6). C. cataphractus with its unique snout shape
filled only 28% of the division. Pairwise comparisons (Table 4.1) showed that C. cataphractus overlaps
morewithC.niloticusthanitdoeswithO.tetraspis.
Table4.1Africancrocodilianspeciespairwisecomparisons
Species Pairwi erlap seov Cor on relati
C.cataphractus niloticus vs.C. 0.46 0.954
C.cataphra vs.O.tetr spis ctus a
.tetraspisvs.C.niloticus
0.38
0.34
0.898
0.985 O
Figure4.6PiechartsshowingthemorphospaceoverlapofthethreeAfricancrocodilianspecies
26
Cuba
The crocodiles of Cuba, originally Crocodylus rhombifer and Crocodylus acutus, had an overlap of 50%
(Figure4.7).WhenC.crocodiluswasintroducedtheoverlapthenincreasedto74%(Figure4.8),meaning
74% of available space is competed for. C. rhombifer and C. acutus were less similar (corr. =0.959,
p=0.01)thanC.rhombiferandC.crocodilus(corr.=0.977,p=0.01).C.crocodiluswasevenlesssimilartoC.
acutus (corr.=0.946, p=0.01). Overlap between native species and introduced show higher overlap
betweenC.rhombiferandC.crocodilus(38%)thanC.acutusandC.crocodilus(33%).
25
Figure4.7PiechartsshowingthemorphospaceoverlapofthetwocrocodilespeciesnativetoCuba
Figure4.8PiechartsshowingmorphospaceoverlapofcrocodilespeciesinhabitingCubaaftertheintroductionofC.
crocodilus
Discussion
Inthisanalysis,weassumedthatdifferenceinsnoutshapewouldincreasenichesegregationandthatthe
craniumshapepredicts,atleastinpart,whatcompetitioncanbeexpectedifmultiplespeciesinhabitthe
samelocation.Whiletheskullhasproventobeamajorecomorphologicaltrait(Busbey1995;Eriksonet
al. 2003), there might be other factors such as habitat availability, nesting preference, population
densities,andbehaviorthatarenotreflectedinskullshape.Thisstudyestimateddirectoverlapofniche
spacebetweenadultspecimens,andtheoverlapcouldchangewhenconsideringhatchlingorjuvenilesor
areasoutsideofthesyntopiczone.
Australia
WeexpectedthehighcorrelationbetweentheAustralianspeciesasbothspeciesbelongtotheCrocodylus
group and genetic evidence suggests a relatively recent separation between them (FitzSimmons et al.
2001). As morphospace translates into niche, these two would experience some competition for
resources, habitat overlap, or general interaction; however, C. porosus is the apex predator due to its
larger adult size and physiological specializations. C. porosus has a widerange throughout most of
Australasianwaters.Itsabilitytowithstandhighsalinityallowsuseofbothfreshandsaltwaterhabitats.
While C. johnsoni tolerates saltwater for short periods, it cannot maintain its health in highly saline
conditions (Taplin et al. 1993), giving C. porosus a physiological adaptation which would increase its
t fav
27
amoun o ailablehabitat.
Webb et al. (1983) noted that the number of C. johnsoni sightings negatively correlated with a recently
conserved and growing population of C. porosus within a zone of syntopy. The relationship Webb et al.
(1983)predictedwasthatC.johnsonipopulationswoulddecreaseby0.79foreachadditionalC.porosus.
This study showed a similar impact predicting that for every one C. porosus, 0.59 C. johnsoni would be
able to coexist (leaving 0.41 outcompeted) if morphospace translates into niche segregation. The visual
countofWebbetal.(1983)gaveacasestudyexamplewheretheactualpresenceoftheanimalaccounts
for factors of competition unforeseen solely from skull morphometrics such as basking location and
26
nesting site availability. However, both studies showed a consequential relationship for C. johnsoni in
directcoexistencewithC.porosus.
India
InthecomparisonofG.gangeticusandC.palustris,wefoundahighoverlapinmorphospaceinasituation
where head shapes are quite different. This was likely due to large size differences in our small sample.
However,thedifferencebetweenthesetwospecieswasnotableinthelowercorrelation,translatinginto
lessnicheoverlap,asG.gangeticusisspecializedasprimarilyafisheater.Otherstudiesindicatedahigher
proportion of G. gangeticus to C. palustris, suggesting that the specialist is surviving better due to depth
andflowofriverhabitatbeingunsuitableforC.palustris(WhitakerandDaniel1980;RaoandChoudhury
1992).Whilethereisoverlapinnestingseasonandsite,andalsohabitat,thereisadistinctionbetween
baskingsiteandfoodpreference(RaoandChoudhury1992).Thesympatrybetweenthesetwospeciesis
stillinneedof urtherinvestigationwithrespecttotheecologicalfactorsthatdistinguishthem. f
SouthAmerica
While there are several species in South America, this research focused on two of the larger and more
common species of caiman, C. crocodilus and M. niger. Since these two species retain similar
morphological characteristics, there was a high overlap in morphospace; therefore, we predicted a high
level of competition between them. Caimans divide their niche in microhabitat use (Herron 1994).
However,nicheoverlapandcompetitionmayaffectthesuccessofconservationeffortsfocusedononeof
asympatricspeciespair.Herron(1994)foundsimilarnumbersofeachspecies(97,C.crocodilusto111,
M. niger) differing from this study which predicted a ratio of 46:54, M. niger to C. crocodilus, which
suggeststhatsnoutmorphologyonlypartiallyexplainsactualnicheoverlapinnature.Wepredictedthat
if conservation measures were to increase C. crocodilus numbers, this would affect the number of
sympatric M. niger. However, many populations of these sympatric species have a higher density of M.
niger, which at current densities has not effected the ecology of C. crocodilus (Marioni et al. 2008). The
interaction between these two species could also be affected by the presence of other crocodilians (see
RebloandLugli2001).
Africa
The overlap calculated for the African species was small. The physical specialization of C. cataphractus
andthesmallsizeofO.tetraspisrendertheselowcompetitorsforC.niloticus,whichistheapexpredator
among the African species. What was of note was the high overlap between C. cataphractus vs. O.
tetraspis despite a lower correlation. This was likely due to C. niloticus outcompeting the others for
resources and space by virtue of its larger size and lack of specialization. In a survey study of African
species in Liberia (Kofron 1992), the lakes inhabited by C. niloticus lacked the other two species. In
contrast, a lake free of C. niloticus had both species and observed moreC. cataphractus than O. tetraspis.
AnotherstudyinGabonandCongo(Eaton2008)foundthatO.tetraspisusesbothaquaticandterrestrial
habitats and thus could occupy a wider range than its sympatric species. C. niloticus preferred coastal
areas, but overlapped considerably with O. tetraspis, while C. cataphractus remained in localized
freshwaterareas.Thissupportstheresultsofthisstudy.Fromthemorphospaceanalysis,C.niloticusand
O.tetraspiswouldbeinmoredirectcompetition;howeverwiththelargersizeofC.niloticus,O.tetraspis
would be a more effective competitor to a specialist such as C. cataphractus or, as one study found, Nile
monitorsVaranusniloticusornatus(Luisellietal.1999),ananimalmorecloselyrelatedinsize.
28
Cuba
The group of coexisting crocodiles in Cuba showed the effect of an introduced competitor. The native
crocodiles, C. rhombifer (endemic and very endangered) and C. acutus were already in competition, as
evidenced by the relatively high overlap in morphospace between these two species. Human pressures
(hunting,habitatencroachment,etc.)furtherlimitedtheirsharedresourcesandhaveevenmadeC.acutus
endangered in Cuba (Varona 1987). The addition of a third crocodilian is predicted to further limit the
amountofmorphospaceand/ornichespaceinhabitablebythreeapexpredators,causingmoredeclinein
C. rhombifer. Ross (1998) already suggested introduction of C. crocodilus as a significant factor for the
extirpated population of C. rhombifer in Lanier Swamp, one of the last remaining wild populations. The
lowersimilarityandoverlap,andhabitatseparation,between C.acutusandC.crocodilusindicateslower
27
competition between these two species leaving C. rhombifer to bear the brunt of resource and space
limitations.
Conclusions
Competition is derived from several ecological and physiological components. While we have not
considered ecology, behavior, physiology and anatomy in these overlap analyses, the head shape alone
appears to offer insight on the niche structure of sympatric species of crocodiles, that have been
confirmed by some ecological or population surveys (Kofron 1992; Webb et al. 1983; Whitaker and
Daniel 1980). The overlap analyses were developed assuming direct interaction; however, as an apex
predator,crocodiliansdriveecosystemchange(Terborghetal.1999)andcompetitiveinteractionsexert
effects outside the area of syntopy. Understanding these effects may inform conservation and
management practices. On a larger timescale, evolution has played a role in the ecological relationships
thatcurrentlyexistbetweenextantspecies(Ross2004).Thesamemethodscouldbeusedtopredictthe
relationships between extinct crocodiles as well, even to the extent of predicting extinction factors
leadingtospeciationandrecentrostrashapeincoexistingspecies.Thismethoddoeslackinformationon
wherethethresholdofminimaleffectsbreaksbetweensympatricspecies.However,newinsightsintoa
basicinteractiononanylevel,extinctorextantcouldbeassessedusingasimilarmethod.
Acknowledgements
Zeno Wijtten for assistance in data collection and analysis, manuscript review and graphics. Dr. Perran
Rossformultiplemanuscriptreviewsandadvice.AmsterdamZoologicalMuseum,RoyalBelgianInstitute
ofNaturalSciences,SeckenbergNaturalHistoryMuseum,Musumnationald'HistoirenaturelledeParis,
and Naturalis Museum, Leiden, The Netherlands, for access to crocodilian skull collections. Franklin D.
RossandProf.dr.MichaelRichardsonforacademicadvice.
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BusbeyIIIA(1995)The structural consequences of skull flattening in crocodilians. In: J Thomason (Ed):
ebrat 1 Functional Morphology in Vert e Paleontology. Cambridge University Press, Cambridge, pp 73-192
Compton TJ, Drent J, Kentie R, Pearson GB, van der Meer J, Piersma T (2007) Overlap in the feeding
morphology of bivalves from speciesrich and speciespoor intertidal flats using gill:palp ratio for
13220 comparativeanalysesofmolluskassemblages.MarineEcologyProgressSeries348:2
EatonM(2008)Conservationandsustainablemanagementofthedwarfcrocodile(Osteolaemustetraspis)
incentralAfricanforests.AfinalreporttotheRuffordFoundationandSmallGrants
Erikson GM, Lappin AK, Vliet KA (2003). The ontogeny of biteforce performance in American alligators
(Alligatormississippiensis).JournaloftheZoologicalSocietyofLondon260:317327
FitzSimmonsNN,TanksleyS,ForstnerMRJ,LouisEE,DaglishR,GrattenJ,DavisS(2001)Microsatellite
markersforCrocodylus:newgenetictoolsforpopulationgenetics,matingsystemstudiesandforensics.
nGCGrigg,FSeebacher,CEFranklin(Eds):Crocodilianbiologyandevolution.SurreyBeatty&Sons, I
ChippingNorton,pp5157
GreerAE(1974)Onthemaximumtotallengthofthesaltwatercrocodile(Crocodylusporosus).Journalof
Herpetology8(4):381384
m i andCai anCrocod lus,inaPeruvianlake.JournalofHerpetology28(4):508513
Kofron CP (1992) Status and habitats of the three African crocodiles in Liberia. Journal of Tropical
Ecology8(3):265273
Luiselli L, Akani GC, Capizzi D (1999) Is there any interspecific competition between dwarf crocodiles
(Osteolaemustetraspis) and Nile monitors (Varanus niloticusornatus) in theswampsofcentralAfrica?A
studyfromsoutheasternNigeria.JournalofZoology247:127131
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Marioni B, Da Silveira R, Magnusson WE, Thorbjarnarson J (2008) Feeding behavior of two sympatric
caiman species, Melanosuchus niger and Caiman crocodilus, in the Brazilian Amazon. Journal of
RaoRJ,ChoudhuryBC(1992)SympatricdistributionofgharialGavialisgangeticusandmuggerCrocodylus
nIn a 9 ) palustrisi dia.JournaloftheBomb yNaturalHistorySociety8 (3 :312315

Rasband WS (19972009) ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA,
http://rsb.info.nih.gov/ij/
ebloGH,LugliL(2001)Distributionandabundanceoffourcaimanspecies(Crocodylia:Alligatoridae) R
inJaNationalPark,Amazonas,Brazil.RevistadeBiologaTropical49(34):10961109
ossJP(1998)Crocodiles:statussurveyandconservationactionplan.2
nd
Edition.IUCN/SSCCrocodile R
SpecialistGroup,IUCN,Gland,Switzerlandp96
Eds):CrocodilianBiologyandEvolution.SurreyBeattyandSons,ChippingNorton,NSW,Australia,pp1 (
2
TaplinLE,GriggGC,BeardL(1993)OsmoregulationoftheAustralianfreshwatercrocodile,Crocodylus
ohnstoni,infreshandsalinewaters.JournalofComparativePhysiologyN:Biochemical,Systemic,and
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Terborgh J , Estes J A, Paquet P, Ralls K, Boyd-Heger D, Miller BJ (1999)InMESoul,JTerborgh(Eds):

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acutusinCuba.Cari Journalo VaronaLS(1987)ThestatusofCrocodylus bbean fScience23(2):256259
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Whitaker R, Daniel JC (1980) The status of Indian crocodilians. Journal of the Bombay Natural History
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Woodward AR, White JH, Linda SB (1995) Maximum size of the alligator (Alligator mississippiensis).
JournalofHerpetology29(4):507513
30
29
Chapter5
ConfirmingSkullMorphospaceasIndicativeofEcologicalNicheProperties
Abstract
In this chapter, I examine the allometric relationships of the skull to the body by using a variety of
measurementstoinvestigatehowvariousphysicalcharacteristicsmayrelatetohabitatandnicheuse.By
examining two crocodiles C. porosus and C. mindorensis with differing ecology, I made inferences to the
functional implications of differing morphology in separating niche. The allometric relationships found
gavesomeimportancetohindlimblength,whichisarguedtobebothimportantinhabitatpreferenceand
possiblynesting.Throughthisandotherrelationships,Igavesupportandinsightintotheeffectivenessof
usingskullmorphospaceanalysistoindicaterealizedniche.
Introduction
The morphology of an organism represents a relationship between the organism and its environment
(Ricklefs and Miles 1994). Playing off this relationship, we can determine interspecific similarities or
differences, especially when making inferences to ecology. When comparing crocodilians, the ecological
aspects which separate them most effectively into species could be evaluated to emphasize factors of
niche segregation. Differentiating ecological niche are prey preference, habitat preference and nesting
type(Ouboter1996).Allofthesetraitsrelate,inonewayoranother,toamorphologicalcharacteristicof
r r crocodilians(Tho bjarnarson1996;Busbey1995;We muth1964).
Snout shape has an obvious relationship with food preference as it is the functional unit for feeding
(Busbey 1995), and the kind of prey consumed likely influences the shape of the snout (Ouboter 1996).
ThisisnotedintheslendersnoutedcrocodilessuchasG.gangeticusandT.schlegelii,whicharespecialist
predators feeding almost exclusively on fish, while other stouter snout shapes have a more varied diet.
Snout shape can also give insights to habitat type. Slendersnouted species tend to inhabit rivers, while
broadsnouted prefer stagnant marshes (Ouboter 1996). This can be interrelated with prey choice;
marsheswouldinhibitcatchingagilefishforaslendersnoutedcrocodile,whilebroadsnoutedprey(e.g.
snails and turtles) are not as abundant in rivers (Ouboter 1996). Rao and Choudhury (1992) also
suggested hydrodynamic shape being a significant factor for slendersnouted species associating more
withrivers.
Thetailshapeandsize,beingassociatedwithlocomotion,canindicatemoreterrestrialoraquatichabitat
type preference. More aquatic crocodilians frequently have longer tails than those that move over land
(Wermuth 1964). Although scientists have not linked ecological niche properties to limb morphology in
crocodilians,itisnotunlikelythatarelationshipexists,butlimiteddataisavailable(Ouboter1996).This
link has been established in other animals such as lizards, fishes and birds (Bourke et al. 2005; Elstrott
andIrschick2004;Leisleretal.1989).
Morphologyaffectsreproductiontotheextentthatphysicalcharacteristicsmightdefineorlimitfecundity
and nest form. Egg size, clutch size and clutch mass positively correlate with female body size
(Thorbjarnarson 1996; Hall 1991). Despite these relationships, very few inferences have been made
concerning the ecological aspects of reproduction such as nest type and nest material. Nesting habits
derive from the habitats in which crocodilians live and the resources available for nest building.
According to Thorbjarnarson (1996), even habitat preference as it relates to nesting needs should be
visible within the morphology of the crocodile. The proportions of the skull should be an indication
(correlatedwith)themorphologyofotherbodypartsandthereforeserveasanindicatororproxyforthe
31
evaluationofthemorphologicalniche.
Itiswidelyacceptedthattheskullisindirectallometrywiththerestofthebody(Greer1974;Woodward
etal.1995)andcandirectlyorindirectlyaccountfornichesegregationincoexisitngcrocodilians(Pierce
etal.2008).Theskullisindicativeofbodysize(WhitakerandWhitaker2008)andrepresentsaphysical
difference between species. Rarely has it been linked to limb or other body parts. In this chapter, I
examine the assumption presented in Chapter 4 that a high percentage of ecological competition is
accountedforwithinthemorphospaceoverlapanalysisofsympatricspecies.
30
Studyspecimens
IusedthecrocodilesofthePhilippines,CrocodylusmindorensisandC.porosus,asstudyspecimens.They
differ ecologically and thus are rarely in direct sympatry. C. porosus is one of the most aquatic of
crocodilian species (Wermuth 1964), while C. mindorensis is more terrestrial, even being found in
mountainous regions uninhabited by C. porosus (Manalo 2008). In accordance with this distinct habitat
difference,thereisadifferenceinpreyitems.Thismayalsobeaproductofsize,asC.porosuscanreach
lengths of 7 meters, while C. mindorensis can only grow to 3 meters (CSG 2008). Both species are,
however,moundbuilders,evenusingsimilarnestmaterialwheninsimilarhabitats(Ouboter1996).This
similarityreducesnichesegregation.
Whilesharingsomeecologicalsimilarities,thetwospeciesaredifferentenoughtocompareforevaluating
theuseofskullmorphospaceanalysisasindicativeofecologicalnichedivision.Byexploringrelationships
between the skull and other physical characteristics, which relate to habitat preference and nesting, I
show the skull to be representative of factors which may induce competition or niche overlap in
coexistingcrocodilianspecies.
Methods
I measured captiveborn, subadult to adult C. mindorensis (N=30) and subadult C. porosus (N=30) at
Davao Crocodile Park, Davao, Philippines. The crocodiles camefrommultiple clutches. Usingasofttape,
measurements were across the body from pointto point. I collected a total of thirteen measurements
fromeachspecimen(Figure5.1ac):cranialwidth(CW),totalskulllength(TSL),hipwidth(HW),length
oftail(TL),snoutventlength(SVL),andforelimblength(FLL)andhindlimblength(HLL)measurements
foreachleg.Cranialwidthwasatthewidestpartofthequadratojugalbone.Headlengthwasfromthetip
ofthesnouttotheposteriorendofthecranialtablealongthemidline.Imeasuredeachlimbseparately,
from the shoulder socket to the carpus. For use in analysis, I calculated the averages between both
forelimbsandbothhindlimbs.Iwastheonlyobservertoreducebiasbetweenmeasurementlocationson
eachindividual.
32
31
a) b)
c)
Figure 5.1(ac) shows locations of measurements recorded from C. mindorensis and C. porosus. 1a shows the
positionsofthelimbmeasurements(HLLandFLL)takenfromtheshoulder/hiptotheendofthelimb,excludingthe
foot and hip width, taken posterior to the hind limbs. 1b shows the measurements taken within the skull including
cranial width (CW) and total skull length (TSL). 1c shows the dorsally measured snoutvent length (SVL) and tail
length(TL).
I conducted a Principal Component Analysis to relate the two study species based on the above
mentioned measurements using PAST (Hammer et al. 2001). I correlated (Pearson) measurements of
cranial width to hip width, limb length, and tail length using SPSS 16.0 and compared the results to
ecological information gathered from literature. For determining relationships between head width and
other measurements of both species combined, I conducted multiple linear regressions, also using SPSS
16.0andincludedfollowupanalysesbasedonresults.
Res
All C. porosus were subadults of similar size (average SVL=90.97cm with a standard deviation of 4.8). C.
mindorensiswerefromjuveniletoadultwithanaveragesnoutventlengthof101.91cm(SD=14.66).
ults
33
32
I evaluated the differences between C. porosus and C. mindorensis using a Principal Component Analysis
(Figure5.2).ThetwospeciesdividedalongPC1(80.44%),whichwasdrivenbydifferencesintaillength
(caseloading:0.744)andSVL(0.519).TheratioofTLtoSVLofC.porosus,onaverage,washigher(1.35)
thanC.mindorensis(1.20),whichaccountedforthespeciesseparationinthePCA.
Figure5.2PrincipalComponentAnalysisshowingthedivisionbetweenC.mindorensisandC.porosusbasedonbody
andheadmeasurements.
Crocodylusporosus
able5.1MeasurementcorrelationsfromC.p us T oros
L CW TSL HW T FLL
TSL Corr. *0.527
Sig. 0.003
HW Corr. *0.673 *0.589
Sig, 0.000 0.001
TL Corr. *0.790 *0.568 *0.733
Sig. 0.000 0.001 0.000
FLL Corr. *0.733 *0.591 *0.616 *0.761
Sig. 0.000 0.001 0.000 0.000
HLL Corr. *0.678 *0.553 *0.599 *0.648 *0.671
Sig. 0.000 0.002 0.000 0.000 0.000
*Corr.Sig.At0.1level(2tailed)

AllmeasurementsfromC.porosusstronglycorrelated(Table5.1).Thosethatcorrelatedsignificantlywith
cranialwidtharethetaillength(corr.=0.790,p=0.001)andforelimblength(corr.=0.733,p=0.001).
34
33
Crocodylusmindorensis
able5.2Meas entc ations mind nsis T urem orrel
SL
ofC.
W
ore
L CW T H T FLL
TSL Corr. *0.624
Sig. 0.003
HW Corr. *0.674 *0.850
Sig, 0.000 0.001
TL Corr. *0.642 *0.659 *0.797
Sig. 0.000 0.001 0.000
FLL Corr. *0.726 *0.567 *0.685 *0.845
Sig. 0.000 0.001 0.000 0.000
HLL Corr. *0.710 *0.676 *0.775 *0.859 *0.765
Sig. 0.000 0.000 0.000 0.000 0.000
*Corr.Sig.At0.01level(2tailed)

Despite the varying sizes of C. mindorensis specimens, all measurements significantly correlated (Table
5.2).Themoststronglycorrelatedmeasurementswerebetweenthelimblengthsandthetaillength,the
hipwidthandthetotalskulllength,hipwidthandtaillength,andhindlimblengthandthehips.
Allometricrelationships
In order to define relationships between measurements within each specimen, I ran a linear regression
analysis.Preliminarylinearregressionvaluesshowedthattheindependentvariablesofhipwidth,snout
ventlength,andaverageforeandhindleglengthrelatetoheadwidth(Figure5.3).Theweakerallometric
relationshipswereduetothecombinationofspeciesinanalysis,showingthatthereisadifferenceinsize
betweenthetwospecies.
Figure5.3Scatterplotshowinglinearrelationshipsbetweenheadwidthandotherbodymeasurements(hipwidth,
snoutventlength,taillength,averageforeandhindleglength)inbothC.porosusandC.mindorensis
Whenfurtherinvestigatingtherelationship,amultiplelinearregressionfoundthatthevariableschosen
could account for the variability within the head (ANOVA: n=60, df=4, F=4.149, p< 0.00), with a large
portion of the variability explained (|= 0.566). Of the variables used, only SVL had a significant
elationshiptoheadwidth(ttest:t=2.142,p=0.119)(Table5.3). r
35
34
Table5.3Coefficientsofheadwidthinamultiplelinearregressionanalysisshowingsignificanceofrelationships
etweenheadwidthandothervariables. trelation ipcanonly oundwithSVL. b Asignifican sh bef
B St r d.Erro t Sig.
(Constant) 6.003 2 .902 2.069 .043
Hipwidth .259 .258 1.00 7 .319
Taillength .031 .027 1.140 .259
SVL .162 .067 2.412 .019*
Avgforelimb .157 .120 1.314 .195
Avghindlimb .042 .093 .446 .657
DependentVariable:headwidth
With the relationship between SVL and head width established, followup analyses determined the
relationships between SVL and other characters (Table 5.4). The multiple linear regression model was
significant (ANOVA: n=60, df= 4, F=82.98, p<0.00). The variables chosen explained 85 % (|) of the
variance within SVL. The strongest characteristics influencing SVL were hip width (t= 5.12, p<0.00) and
taillength(t=3.57,p<0.00).

Table 5.4 Coefficients of SVL in a multiple linear showing significance of relationships between SVL and hip width,
aillengthandaverageforeandhindlimblen ant relationshipsaremarkedwithanasterisk. t gth.Signific
B St r d.Erro
(Constant) 26.298 4.648 5.657 .000
Hipwidth 2.187 .427 5.117 .000*
Taillength .178 .050 3.566 .001*
Avgforelimb .402 .236 1.706 .094
Avghindlimb .094 .188 .497 .621
DependentVariable:SVL

The strong relationship between hip width and SVL led to the testing of the hips in relationship to tail
length,averageforelimblengthandaveragehindlimblength(Table5.5).Theresultsshowedasignificant
relationship between the hindlimb length and the hips (t= 5.70, p<0.00). The linear regression analysis
was significant (ANOVA: n=60, df=3, F= 63.573, p<0.00), accounting for a high percentage of variability
withinhipwidth(|=0.77).

Table 5.5 Coefficients of hip width from a multiple linear regression analysis showing significant relationships
etweenhipwidthandoth physicalc cs.Avera dlimblength astheon nificantvariable. b er haracteristi gehin w lysig
B St r d.Erro Beta t Sig.
(Constant) .850 1 .462

.581 .563
Taillength .007 .016 .039 .455 .651
Avgforelimb .136 .072 .245 1.894 .064
Avghindlimb .269 .047 .689 5.700 .000*
DependentVariable:hipwidth

36
35
I used an independent samples ttest to compare hindlimb lengths between species. C. mindorensis had
significantlylongerhindlimbsthanC.porosus(t(59)=7.15,p<0.00).
Discussion
In order to show the skull as representative of niche, an encompassing ecological trait needed to be
identified.Iusedhabitatpreferenceasitisinclusiveofseveralecologicalnichefactors.Forexample,type
ofpreyisinterrelatedwithhabitatascrocodilianscanonlypreyonwhatisavailablewithintheirhabitat
(Ouboter 1996). The skull is the feeding apparatus and thus accounts for preferences in diet (Busbey
1995). Habitat preference also includes nesting preferences as material necessary to build nest, either
moundorburrow,arewhatisavailablewithinthehabitat(e.g.Cott1961;Webbetal.1983).
ThePhilippinesspeciesarevariantenoughinsizeandecology,whilesimilarinskullshape,tolendsome
insights to the effectiveness of using skull morphometrics as representative of niche dynamics. The
measurements deciphered between species as shown through the principal components analysis and
within the allometric relationships as the relationships were weaker when anlaysing both species
together. The allometric relationships positively correlated between cranial width and the other
measurements of SVL, TL, HLL, FLL, and HW. I also confirmed that the measurements significantly
correlatewithinspecies.
Whenrelatingtheskulltoecologicaltraits,relationshipsbetweentheskullandfunctionalmorphological
characteristics need to be established. In the C. porosus specimens, the cranial width significantly
correlatedwithtaillengthandtheforelimb.Bothofthesearetraitsareinformativeabouthabitatuseas
explained later. Within the C. mindorensis specimens, all physical characteristics significantly correlated
tocranialwidth.
Aftertheallometricrelationshipswereestablished,IexplainedthevariabilitywithinCWmeasurements,
using SVL, TL, HLL, FLL, and HW. SVL explained the variance in CW. I expected the direct and strong
relationship between skull shape and SVL proportions, as it is defined allometric growth in crocodilians
(Greer 1974; Woodward et al. 1995). With this relationship well established, I related other physical
characteristics(HLL,FLL,TL,HW)toSVL.HipwidthandtailwidthdrovethevariancewithinSVL.The
tail is used to balance out the body when erect on land (Frey 1988) and therefore would need to be
stronglycorrelatedwith(inproportionto)SVL.
The hips were also proportional to the skull. Hip width is not an ofteninvestigated functional
measurementincrocodiliansandthereforewasexplored.Iexplainedthevarianceinhipwidthusingthe
remaining measurements of TL, FLL and HLL showing hindlimb length to be the driving force of the
variance. The hindlimb lengths significantly differed between species, with C. porosus having shorter
t speciesthr v limbs.Thismaybedue othedifferenthabitatsinwhichthesetwo i e.
Habitat preference of the two species is markedly different. C. porosus is found in more aquatic
environments.Thiscorrelateswithitslongmusculartailusedforpropulsionanditsreducedlimbusefor
streamlining (Seebacher et al. 2003). Whereas C mindorensis is more terrestrial found in mountainous
terrain and would find longer limbs helpful in maneuvering over and around rocks, bushes, thick grass,
etc. Longer legs adapted for terrestrial habitation is most apparent in the physical transformation of
amphibians from water to land (Ivanovic et al. 2008). Licht (1986) showed that frogs with longer legs
preferredtoescapeoverlandthanthosewithshorterlimbs,whichchoseaquaticescape.Longhindlimbs
in lizards suggests enhanced performance in speed and maneuverability over land, especially when
combinedwithshorterforelimbs(Vanhooydoncket.al2000).Thesignificantdifferencebetweenthetwo
crocodilespeciesinhindlimblengthandtaillengthtobodyratiorelatedtoprimaryhabitattypesuggests
that these character traits are indicative of habitat use, at least to the extent of identifying terrestriality.
The tail is a proven indicator of ecology (Wermuth 1964). As these physical characteristics correlate to
37
theskull,theskullitselfisreflective,atleastinpart,ofhabitatpreference.
Other morphological characteristics, which correlate to skull shape, point to other aspects of niche
besides habitat use. Thorbjarnarson (1996) and Hall (1991) previously identified the relationship
betweeneggmassandfemalebodysize.IagainshowedtherelationshipbetweenSVLandtheskull.This
relates skull shape to a reproductive characteristic, strengthening the skulls use for determining niche
segregationinsympatricspecies.Inaddition,IfoundthatthevarianceinSVLwasprimarilyexplainedby
hipwidth.Perhapshipwidthrelatestofecunditythesameasbodysize,eitherthroughclutchsizeoregg
36
size. Hind limb length is also a possible indicator of nesting habits, as many crocodilians use their
hindlegstobuild,dig,orcovertheirnests.
Conclusion
When translating skull morphospace into niche space, the skull does account for a large proportion of
ecological variables which would induce competition between sympatric species. I established hindlimb
lengthasanother characteristic whichcan be related to habitatandproportionately related tothe skull.
Hind limb length, tail length, and other accepted linking characteristics (skull itself and body size to
reproductivecharacteristics)betweentheskullandthehabitat,furthersupportthevalidationoftheskull
as reflective of niche use and therefore niche segregation. This information can be used in husbandry
practices for developing suitable enclosures, but also in directing release programs to ensure release
occursinavailablehabitatbestsuitedforaparticularspecies.Otherspeciesshouldalsobeexaminedfor
relevant relationships and with more information. This study was limited to captive animals and data
fromliterature.Othermeasurementscouldalsobeusedforcomparisonssakesuchasskullsurfacearea,
Klin1212orlimbgirth.
Acknowledgements
Zeno Wijtten for comments and revisions. Franklin D. Ross for measurement considerations. Davao
Crocodile Park for access to and assistance with their crocodiles. Forum on Philippine crocodile
conservationformonetaryassistancefordatacollection.
References:
BourkeP,MagnanP,Rodrguez(2005)Individualvariationsinhabitatuseandmorphologyinbrook
Biology51(4):783794 charr.JournalofFish
BusbeyIII,A(1995)The structural consequences of skull flattening in crocodilians. In J Thomason (Ed):
Functional Morphology in Vertebrate Paleontology. Cambridge University Press, Cambridge, pp173-192
CottHB(1961)ScientificresultsofaninquiryintotheecologyandeconomicstatusoftheNilecrocodile
(Crocodilusniloticus)inUgandaandNorthernRhodesia.TransactionsoftheZoologicalSocietyofLondon
29:211356
ableat:http://iucncsg.or/ph1/modules/Crocodilians/ CSG(2008)Crocodilianspecieslist.Avail
species.html[Accessed11March2010]
ElstrottJ,IrschickDJ(2004)Evolutionarycorrelationsamongmorphology,habitatuseandclinging
performanceinCaribbeanAnolislizards.BiologicalJournaloftheLinneanSociety83:389398
reyE(1988)DasTragsystemderKrokodile:einebiomechanischeundphylogenetischeAnalyse. F
StuttgarterBeitrageNaturkundeA26:160
Hall PM (1991) Estimation of nesting female crocodilian size from clutch characteristics: correlates of
reproductivemode,andharvestimplications.JournalofHerpetology25(2):133141
Hammer,HarperDAT,RyanPD(2001)PAST:PaleontologicalStatisticsSoftwarePackageforEducation
and Data Analysis. Paleontological Electronica 4(1):pp9. http://palaeoelectronica.org/2001_1/past/
issue1_01.htm
IvanovicA,TomasevicN,DzukicG,KalezicM(2008)Evolutionarydiversificationofthelimbskeletonin
crestednewts(Trituruscristasussuperspecies,Caudata,Salamandridae).AnnalesZoologiciFennici
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45:527535
LeislerB,LeyH,WinklerH(1989)Habitat,behaviourandmorphologyofAcrocephaluswarblers:an
integratedanalysis.OrnisScandinavica20:181186
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LichtLE(1986)ComparativeescapebehaviorofsympatricRanaauroraandRanapretiosa.American
7 MidlandNaturalis115(2):23924
ManaloR(2008).OccurrenceofCrocodylusmindorensisintheCordilleraCentral,AbraProvince,Luzon
Island.NationalMuseumPapersSpecialIssue:ProceedingsForumonCrocodilesinthePhilippines14:
109115
PierceSE,AngielcyzkKD,RayfieldEJ(2008)Patternsofmorphospaceoccupationsandmechanical
performanceinextantcrocodilianskulls:acombinedgeometricmorphometricandfiniteelement
palustrisinIndia.JournaloftheBombayNaturalHistorySociety89(3):312315

Ricklefs RD, Miles DB (2004) Ecological and evolutionary inferences from morphology: an ecological
perspective. In PC Wainwright, SM Reilly (Eds): Ecological Morphology: Integrative Organismal Biology,
UniversityofChicagoPress,Chicago,pp1342
Seebacher F, Elsworth PG, Franklin CE (2003) Ontogenetic changes of swimming kinematics in a semi
aquaticreptile(Crocodylusporosus).AustralianJournalofZoology51:1524
ThorbjarnarsonJB(1996)ReproductivecharacteristicsoftheorderCrocodylia.Herpetologica52(1):824
Vanhooydonck B, Van Damme R, Aerts P (2000) Ecomorphological correlates of habitat partitioning in
ert 358368 Corsicanlac idlizards.FuncionalEcology14:
Webb GJW, Buckworth R, Manolis SC (1983) Crocodylus johnstoni in the McKinlay River area, N.T. VI.
Nestingbiology.Australian WildlifeResearch10:607637
Wermuth H (1964) Das Verhltnis zwischen Kopf, Rumpf und Schwanzlnge bei den rezenten
Krokodilen.SenckenbergianaBiologica.45:369385
tGroupNewsletter27(4):2630 WhitakerR,WhitakerN(2008)Whosgotthebiggest?CrocodileSpecialis
WoodwardAR,WhiteJH,LindaSB(1995)Maximumsizeofthealligator(Alligatormississippiensis).
ournalofHerpetology29(4):507513 J
39
38
Integrationofresultsintoaconservationplan
"Unlesssomeonelikeyoucaresawholeawfullot,Nothingisgoingtogetbetter .It'snot."
Dr.Seuss
40
39
Chapter6
AssessingCarryingCapacityforSympatricCrocodilianPopulations
Abstract
With habitat availability being a necessity to the success of crocodilians, I described an equation which
relies on population ecology of sympatric species to determine habitat available for conservation and
management tactics. By this, conservationists are given a simple and applicable way of providing
parameters to their action plans which take into consideration the needs of coexisting apex predators
withinthelimitsoftheirhabitat.
Introduction
Habitat includes several ecological factors and is indicative of the needs for crocodilian survival. It
represents the food source (Ouboter 1996) and influences nesting success (Thorbjarnarson 1996;
Campos 1993). Habitat availability also plays a role in allowing the sympatry of coexisting species,
providing for differences which reduce competition (Ouboter 1996; Herron 1994). Habitat loss is the
single most important factor driving population decline of threatened crocodilians (Ross 1998;
Thorbjarnarson 1999). With the limiting factor of crocodilian population growth so boldly defined, it
would be wise to consider it in conservation and management strategies. Suitable habitat is becoming
less and less available (Thorbjarnarson et al. 2006; Kushlan 1988) and despite crocodilian
resourcefulness,crocodilescannotsurvivewithoutsomebasicrequirements.
Differentiated habitat use results in niche separation between sympatric species. However, especially in
apex predators, niches and habitat use do overlap. When the species under consideration for
conservation is an apex predator, with a limited habitat, conservation efforts directed at one species
might very well affect other species in the area and the usability of the habitat (Sergio et al. 2006). This
becomesevenmoreevidentwhenbothspeciesareapexpredators.
Crocodiliansareapexpredatorswhichsometimesoccurinsympatry.Whenonepopulationinthepairis
manipulated, it will have an effect on the sympatric population (Ouboter 1996). Webb et al. (1983)
deemed a recently conserved population of C. porosus to be having a negative impact on its neighboring
population of C. johnsoni in Australia. Crocodilians within a certain range of each other will probably
shapeeachothersecology,andthereforeconservationactionswithinasharedhabitatmustbeconscious
n e a oftherelationshipsbetweencoexisti gsp cies(Thorbj rnarson etal.2006).
Interaction between habitat type and population ecology provides important consideration for
management and conservation of crocodilians (Thorbjarnarson et al. 2006). This interaction in
crocodilians includes information on home range, group size and abundance. This information can also
oftendirecthabitatneedsofapopulationaswell.Themainobjectiveofconservationisaselfsustaining
population (Griffith et al. 1989). With the acknowledged integration of population and habitat, this
objective can be put into perspective of the needs of the crocodile within the limitations of the
environment.
The aim of the chapter is to present a simple equation which accounts for carrying capacity of the
environment, while being aware of ecological necessities of sympatric crocodilians. In this way, the
equationacknowledgesimpactofbothspecieswithinthehabitat,andinturnspeciesoneachother.With
such a vulnerable species group acting as apex predators, it is of utmost importance to research all
optionsforconservationcarefullyandincorporateasmanyvariablesaspossible,especiallythoserelated
tointerspecificpopulations.
The equation is a working hypothesis from qualitative analysis based on observation and supported by
literature.Literaturesupportstheimportantfactorsindefiningpopulationecologywithintheparameters
of a given habitat. The goal was to remain simple to ensure applicability to as many casescenarios as
possible,whilealsostillofferinginsightfordirectedconservationefforts.
41
40
Methods
I conducted a literature review to determine variables of interest for defining habitat needs of a
population.Iusedliteratureandlogicalrelationshipstodeterminetheaffectsthoseparametershaveon
eachother.Finally,Idevelopedahypotheticalsympatricpopulationsituationtoshowfactorsinfluencing
populationsizeandreproductivesuccessandtheconsequencesofsuccessforthecoexistingpopulation.
I also used information gathered and quantified from Ouboter (1996) to delve into factors affecting the
usability and value of habitat availability. I quantified the information on Caiman crocodilus and
Melanosuchus niger by giving a value range (01 for yes or no; 02 or 03 for levels of difference) to the
differencesinhabitatusecharacteristicofeachspecies.Inthisway,Igavenumericalvaluetothetraitsof
overlap in habitat use. By comparing the similarities, focus points for areas of change (conservation)
couldbeindentified.
Explanationofconstants
The total area available for crocodiles consists of area shared by a pair of sympatric species, area that
they exclude each other from (or that one excludes the other from) and suitable habitat within the
study/conservation site. This is a capricious variable dependent completely on the environment and
thecrocodile.Forinstance,ifariverinespeciesistobeconserved,thenthesquarekilometersofrivers,
plustheprescribedbufferzone(neededforbasking,nesting,etc.)mustbesummedtorepresentthetotal
areainhabitable.Marinespeciessympatricwithfreshwaterspeciesshouldincludeonlythehabitatwhich
iswithinhomerangeofthecoastasopposedtotheentireocean.
A=Aexclusive+Ainclusive+Asuitable
Home range determines the area integral to survival; it is the area necessary for an animal to satisfy its
needsoffood,waterandshelter(Hubbardetal.1998).
HR=homerangeortheareanecessaryforindividualsurvival
Population ecology relates to habitat use and limitations in sympatric species settings. Because of this,
terms of population ecology must be integrated into the equation. HR would begin to overlap in
communal species, thereby reducing the total area necessary for the population. This would then affect
theareavariable(A)andthereforemustbeconsidered.
C=communitysize,whichisthenumberofindividuals/group
Inordertoquantifythearea(A)needed,wemustknowthepopulationsize.
P=populationsize
Idefinehabitatavailabilityastheunusedareaavailableforpopulationmanipulationforconservationor
managementactivity.
HA=habitatavailable
BasicModel
Sympatricspecieswillaffecteachotherandincreaseboththeamountofhabitatusedandimpactonthe
habitat itself. With the following equations, I show how much habitat is necessary for and used by both
42
speciespresent.
Inordertoshowthehabitatneedsofasinglepopulation,homerangeofanindividual(HR)isdividedby
overlap within the group (C). Intraspecific overlap, which here is determined by the average group size,
befits the equation because social behavior cannot be ignored in consideration tosympatric species and
heavily impacts home range. In any coexisting situation, behavior plays a major role both in inter and
intraspecific situations (Garrick and Lang 1977). Species which function as a group are more likely to
withstandthepresenceofotherindividualsorspecies,likeNilecrocodilesCrocodylusniloticusandhippos
Hippopotamus amphibius (Kofron 1993). When applied to estimating space, crocodilians which do not
function in groups will need more space than those that do. Total combined home range of multiple
41
individualswouldbelessiftheyaregroupspecies,thusdividinghomerangeofanindividualbyaverage
upsizeaccountsforthatreductioninnecessaryhabitat. gro
(1) Areanecessarypergroup=HR
1
/C
1
(whereCdoesnotequalC)
With the establishment ofhabitat needsfor a species, the size of the population must be integrated into
the equation. Abundance acts as an indicator for relative success of a species and is necessary to have a
quantitativeapproachinevaluationoflongtermviability(Mazzottietal.2009;Lindenmayeretal.2000).
Thisthengivesthehabitatusebyonepopulation.Inhabitatssupportingmorethanonespecies,habitatin
useforallspeciesmustbedetermined,thereforeP
1
isthesizeofpopulation1,P
2
isthesizeofpopulation
c. 2,et
(2) A
1
=P
1
*HR
1
/C
1
Oncethehabitatinusebyeachpopulationisdetermined,thisissubtractedfromthetotalareaofsuitable
habitat(A).Thisdefineshabitatavailability(HA).Whencombined,theequationshowsHAasaresultof
populationabundance,homerangeandthecommunityoverlapfactorforbothpopulations.
(3)
where P= population abundance, HR= home range (km
2
) and C=community (equivalent to the average
group size), A=area of suitable habitat for crocodilians (km
2
), where A is greater than or equal to
(P
1
*HR
1
/C
1
)(P
2
*HR
2
/C
2
)
I squared and square rooted the population area values, which are subtracted from A, to give a positive
integer. This ensures that a negative number does not cancel the subtraction from the whole (A). An
exampleofhowtousetheequationispresentedinthenextchapter(Chapter7).
Effectswithinconstants
Populationsize
Population size (P) can be altered by several ecological and nonecological factors, which can either
increaseordecreasethenumbersandthesusceptibilitytoimpactbychangeinacoexistingspeciesofthe
population.Forthepurposesofthisdiscussion,Iconsideredonlynaturalandcommonecologicalfactors.
Theslowandsteadyprocessofreproductionistheonlylastingwayofincreasingapopulation(without
reintroduction). The ability to pass on genes is most important for population growth, i.e. the age of
sexualmaturity,andisthefocusofthisdiscussionasaffectingpopulationsize.Reachingtheageofsexual
maturity ensures at least the chance to expand the population. A selfsustaining population marks the
successofaconservationproject(Griffithetal.1989).
Thelowertheageofsexualmaturity,thelesstimerequiredtosurvivebeforereproducing(4and5);this
also gives an ecological advantage compared to the sympatric species, which will have to compete with
the already established offspring. The number of predators capable ofconsumingacrocodile atany life
stageuptotheageofsexualmaturityalsoaffectsthatsurvivalrate(6).Maximumabundanceofaspecies
acer the 6). is,to tainextent,dependanton threatofpredation(Paine196
| ty (4) Ageuntilsexualmaturi +successratetosexualmaturity
(5) +Ageatsexualmaturity 4 +lesstimeneededtosurvivetoreachsexualmaturity|successrate
tosexualmaturity
43
(6) |Numberofpredators+successratetosexualmaturity
Anotherecologicalfactorinfluencingpopulationdensityisreproductivesuccess(7),andthereproductive
success of both coexisting species must be considered. Success rates can increase if mating and nesting
42
seasonareatdifferenttimesforthecoexistingspeciesorifthereisadifferenceinnesttypeasdifferent
materials and locations could be used, as suggested for an increase in the value of habitat. These are
especiallyimportantinareasofdirectoverlap.
(7) PNumberofeggs*estimatednumberofreproductivefemales*#clutches/female/season
If population density increases, it will have a direct effect either on the amount of habitat available, the
s populationdensityofthecoexisting pecies,orboth.
In the example (Table 6.1), I used hypothetical numbers to give an idea of what effects reproductive
successa tions. ndtherepercussionstothecoexistingpopula
Table6.1FactorsaffectingpopulationabundancebetweenSpecies1andSpecies2usinghypotheticalvaluesto
etermineestimatednumberofindividualsreachingsexualmaturity. d
Populationabundance
Numberofeggs/clutch
factors Species1 Species2 Est.effect
Highernumberofeggsgives
tageover 14 10 Species1anadvan
Species2
Est.numberofreproductive
females 45 30
HighernumberofSpecies1
femalesincreaseschanceof
successfuloffspring
#clutches/female/season
3 2
Moreclutchesperseasongives
Species1anadvantageover
Species2
Total#hatchling/season
productofpreviousthree (
factors)
1890 600
Highcompetitionbetween
atchlingsandjuvenilesfor h
survival

Ageofsexualmaturity
10 12
LowerageofSpecies1givesit
higherchanceofpassingongenes
thanSpecies2
#ofpredatorsbeforesexual
maturity
5 5
Equaleffectofpredationonboth
species.However,highnumberof
ufferfor Species1givesmoreb
survivalofsomeoffspring
Successratetosexualmaturity
6% 8%
LowersuccessrateofSpecies1is
bufferedbyhighernumberof
offspringunlikeSpecies2
Total#reachingsexualmaturity
113.4 48
Species1willusethemajorityof
theresourcesavailableinshared
habitat
Other factors may affect population density but with little predictability in occurrence. Hunting and
poaching can have a negative impact on species but rarely take both species in a sympatric situation at
thesamerate(e.g.RebloandMagnusson1983).
44
HabitatAvailability
Habitat availability (HA) is altered through habitat use. The way different crocodilian species use their
habitat may increase the value of the available habitat for use by both species. The obvious factor
increasinglandusabilitywouldbeifthecoexistingpairpreferreddifferenthabitats;thiswouldincrease
theuseofasinglelocationforconservationifbothhabitattypesareavailable.Habitatoffersasignificant
difference between sympatric crocodilian species,as45% of interacting speciespairsarea combination
of a coastal species and a freshwater species (Ouboter 1996). C. acutus and A. mississippiensis occupy
southern Florida but are rarely overlapping as C. acutus prefers coastal habitat while A. mississippiensis
prefers lakes and freshwater to brackish marshes (Ouboter 1996; Ogden 1978). Basking and nesting
43
locations/types can even occur in the same locations if there is a preferential difference in vegetation
and/ormicrohabitatbutwouldnothaveasgreatanimpactasdifferenceinmacrohabitat(Ouboter1996).
Habitat use is also different at different life stages (Halpern et al. 2005), meaning habitat use between
speciesmightonlyconflictduringnestingseason,ashatchlingsofallspeciesneedfreshwaterforsurvival
ofthefirstthreemonths(Ouboter1996).
Differenceintimeofactivitywouldalsoincreasetheuseofalimitedamountofhabitat(Ouboter1996).If
one species is more active at night, then it competes less with diurnal animals. This time niche extends
into mating and nesting seasons as well. As these are usually strenuous times, less interference by a
competing species will help reduce the stresses already caused by intraspecific interactions for mates,
primenestinglocations,andnestprotection.
Another way to increase the value of a habitat is if one species has the physiological capabilities to
withstandeitherhighsalinities(osmoregulation)orlowtemperatures.Eitherofthesecanexpandusable
habitat outside of shared habitats. In turn, those species unable to tolerate these have a limited
environmenttoinhabiteitherbysalinityorbyfreezingtemperatures.A.mississippiensisdoesnotinhabit
estuarine waters in the same capacity as C. acutus because Alligatorids have a limited physiological
tolerancetohighsalinities(MazzottiandDunson1989).
Finally, the carrying capacity of the habitat itself limits habitat availability. Many factors come into play
within carrying capacity, including availability of resources and suitable habitat for each species. The
competition can be reduced based on preferences mentioned above such as habitat, basking location,
nesting, etc. Differing between food items can also increase the carrying capacity of a shared area.
However,asavailablefoodisdirectlylinkedtothehabitat,itisaresultofthehabitatinwhichsympatric
pairslive.Withoutextremespecializations(suchasG.gangeticus),thereislittledifferenceinconsumed
food as most crocodilians are opportunistic feeders. Because of this, biomass is a better indicator of
mentwhere ialistcro carryingcapacityintheenviron spec codiliansarenotpresent(Tayloretal.1990).
Forexample,whencomparingC.crocodilusandM.nigerinanassumedhealthyandsuitableenvironment,
we find an estimated 60% chance of overlap based on ecological characteristic differences (Table 6.2;
quantified from Ouboter 1996). In order to increase the habitat availability, areas of similarity would
have to be the focus for conservation, in this case, focusing on expansion of macrohabitat. Of the 60%
overlap,only13%canbechanged,thusinequation3,habitatavailability(HA)canonlyincreaseby13%
of its starting area, which also limits the change possible in population density. In order to change the
score for macrohabitat, conservation focus could be on habitat encroachment or expansion of natural
parks.
Table6.2TablerepresentingpropertiesresultinginconflictinguseofhabitatbetweenC.crocodilusandM.nigerThe
valuerepresentspossibleranksofinterspecificdifferenceswhilethescoreindicatestheamountofdifference
betweenpresentedspecies(0=greatest ce). differen
V Circumstance alue* Score Canbechanged
Differenceinmacrohabitat? 02 1 Yes
Differenceinmicrohabitat?
nce?
02 1 Yes
Differenceinbaskingprefere
01 1 No
Differenceinnestingsite? 01 0 No
Differenceinnestingtype?
etime?
01
03
1
3
No
No Differenceinactiv
Differenceinnestingseason?
01 0 No
Osmoregulation?
oth=.5) (one=0,neither=1b
01 1 No
Lowtemperaturetolerant?
Specialistpresent?
Biomasssuitablefortwospecies?
01
01
01
0 No
No
Yes
0
0
/15=60% L
*
ikelihoodofoverlapinhabitat 8
wheredifference=0
45
44
However, habitat is most often altered by human impact, so this would decrease the amount of suitable
habitatorcouldevenpartitionthespaceavailable,creatingtheneedforlandbridgesorotherconnective
methods.Thesenecessitiescannotbeaccountedforwithinthisstudy.
Discussion
Habitat is often the limiting factor in conservation projects (Czech 2000; Milsap et al. 1990). In habitats
with sympatric species, habitat use and conservation must be conscientious of both species preferences
and needs. The equation presented is simple with insights into sympatric species, but it can be quickly
applied(Chapter7)togiveageneralideaoftheamountofspaceavailableand/ortheestimatednumber
ofcrocodilesthatahabitatcancarry.
I chose abundance (P), home range (HR), and intraspecific overlap (C) as the important factors in
population ecology of sympatric crocodilian species for use in this study. These encompass many
variablesinsinglevectorsallowingforasimplebutdescriptivemodelofhabitatuse.However,limitations
exist within the equation as it does not describe all facets of population ecology, such as factors
influencingbothpopulationsizeandvalueofhabitatavailability,whichIexplained.
Whilethemodelgivesaroughestimateofareaavailableforexpansion(HA)withoutinfringementonthe
sympatricpopulation,itbecomesmorecomplicatedbyfactorspresentinmultirangeenvironments,e.g.
theverylimitedhabitatofC.rhombifercomparedtoitswiderangingsympatricspeciesC.acutus(DeSola
1930). This can, however, be accounted for in that most conservation projects focus on a very specific
area, for example the conservation of C. mindorensis in the Linguasan marsh, Mindanao, the Philippines
(Ross1984).
Anotherlimitationoftheequationisthatitisimpossibletoknowinwhichdirectionandintowhatspace
a population will expand, although it can be assumed that it will expand in the direction with least
resistance (St. Amant 1970). This is important in areas of unequal population distribution, especially
whereonepopulationissignificantlylargerthantheother.Thereisalsonowaytogivevaluetothespace
betweenneighboringpopulations.Ifcoexistingpopulationsdonotoverlap,thanthespacebetweenthose
populations becomes far more valuable as space for population expansion of one species without
interferingwiththecoexistingpopulation.
Conclusion
Availabilityofsuitablehabitatisworldwidethelimitingfactorforhealthycrocodilepopulationgrowth.It
shouldthereforebeanimportantfocusinconservationandmanagementtacticsandevenmoresowhere
conservation or management involves sympatric species. Sympatric species will have an effect on each
other and increase both the amount of habitat used and the impact on the habitat itself. It is best to
understandhowmuchhabitatisnecessaryandusedforbothspeciespresent.
Whencreatingaconservationplanformultipleapexpredatorenvironments,thecoexistingspeciesmust
be comparedtoassess each species advantagesanddisadvantagesto survivaland successascompared
to its sympatric species. In this way, we can determine focus areas for conservation or management
tactics,whichhaveaminimalnegativeimpactonsympatricpopulation.Conservationistsdeterminefocus
areas through the assessment of the value of the habitat which increases or decreases by what it has to
offer for the survival of both species. Assessment of biases for survival of one species over the other
within the same habitat also lends insight into the carrying capacity of a given area. Where populations
are not syntopic, the focus of conservation lies in the space between the populations to make sure this
area is suitable to the presence of both species. Therefore, both species benefit when their share of the
environment and ecological characteristics is acknowledged within the confines of suitable habitat
available.
In general, giving conservationists an equation by which to estimate available space for population
expansion without or with limited consequences to a neighboring, sympatric population will benefit
planningandimplementationofprojects.Italsogivesafocusareaforsuccessandamethodofevaluation
ofinteractionwithinconserved,sympatriccrocodilianpopulations.
46
45
References:
Campos Z (1993) Effects of habitat on survival of eggs and sex ratio of hatchlings of Caiman crocodilus
yacareinthePantanal,Brazil.JournalofHerpetology27(2):127132
Czech B (2000) Economic growth as a limiting factor for wildlife conservation. Wildlife Society Bulletin
28(1):415
DeSolaR(1930)TheCubancrocodile:anaccountofthespeciesCrocodilusrhombiferCuvier,withnotes
onitslifehistory.Copeia1930(3):8183
Garrick LD, Lang JW (1977) Social signals and behaviors of adult alligators and crocodiles. American
Zoologist17(1):225239
GriffithB,ScottJM,CarpenterJW,ReedC(1989)Translocationasaspeciesconservationtool:statusand
strategy.Science,NewSeries245(4917):477480
Halpern BS, Gaines SD, Warner RR (2005) habitat size, recruitment, and longevity as factors limiting
populationsizeinstagestructuredspecies.TheAmericanNaturalist165(1):8294
andCaimancrocodilus,inaPeruvianlake.JournalofHerpetology28(4):508513
KofronCP(1993)BehaviorofNilecrocodilesinaseasonalriverinZimbabwe.Copeia1993(2):463469
KushlanJA(1988)ConservationandmanagementoftheAmericancrocodile.EnvironmentalManagement
12(6):777790
Lindenmayer DB, Margules CR, Botkin DB (2000) Indicators of biodiversity for ecologically sustainable
forestmanagement.ConservationBiology14(4):941950
MazzottiF,DunsonW(1989).Osmoregulationincrocodilians.AmericanZoologist29:903920
MazzottiFJ,BestGR,BrandtLA,CherkissMS,JeffreyBM,andRiceKG(2009)Alligatorsandcrocodilesas
indicatorsforrestorationofEvergladesecosystems.EcologicalIndicators9(6):S137S149
Milsap BA, Gore JA, Runde DE, Cerulean SI (1990) Setting priorities for the conservation of fish and
. wildlifespeciesinFlorida WildlifeMonographs111:357
Ogden JC (1978) Status and nesting biology of the American crocodile, Crocodylus acutus (Reptilia,
Crocodilidae)inFlorida.JournalofHerpetology12(2):183196
n alist100:6576 PaineRT(1966)Foodwebcomplexitya dspeciesdiversity.The AmericanNatur
Reblo G, Magnusson W (1983). An analysis of the effect of hunting on Caiman crocodilus and
sc c Melanosuchusnigerbasedonthesizesofconfi atedskins.Biologi alConservation26:95104
Ross CA (1984) Crocodiles in the Republic of the Philippines. In: Crocodiles. Proceedings of the 6
th
, WorkingMeetingoftheCrocodileSpecialistGroup,IUCN/SSCGland,Switzerland pp.8490
nd
Specialist GroupIUCN,Gland,SwitzerlandandCambridge,UK
Sergio F, Newton I, Marchesi L, Pedrini P (2006) Ecologically justified charisma: preservation of top
predatorsdeliversbiodiversityconservation.JournalofAppliedEcology43:1049105
St.AmantJ(1970).Thedetectionofregulationinanimalpopulation.Ecology51(5):823828
47
46
Taylor D, Aarssen L, Loehle C (1990). On the relationship between r/K selection and environmental
carryingcapacity:anewhabitattemplateforplantlifehistorystrategies.Oikos58:239250
ThorbjarnarsonJ(1996)ReproductivecharacteristicsoftheorderCrocodylia.Herpetologica52(1):824
ThorbjarnarsonJ,MazzottiF,SandersonE,BuitragoF,LazcanoM,MinkowskiK,MuizM,PonceP,Sigler
L, Soberon R, Trelancia AM, Velasco A (2006) Regional habitat conservation priorities for the American
36 crocodile.BiologicalConservation128:25
ustralianWildlifeResearch10:639650 A
48
47
Chapter7
FromSkullShapetoConservation:M.nigerandC.crocodilus
Abstract
Through the combination of skull morphospace analysis and ecological characteristics, I determined a
guidingmodelforapplicationoftheskullmorphospaceanalysistocrocodileconservationusingliterature
studiestocreateanexample.TheresultsshowedthepopulationratiobetweenM.nigerandC.crocodilus,
underhabitatlimitedcircumstances,tobefarfromtheestimatedequilibriumthushinderingpopulation
expansion of C. crocodilus by M. niger. I discussed ecological characteristics which increase the value of
the habitat available. While only an example study, I gave suggestions for manipulating resources to
encouragepopulationstoreachanequilibriuminordertoensuresuccessinbothpopulations.
Introduction
Populations of different species occupying or using overlapping geographical areas, without
interbreeding are sympatric. When both species have similar ecology, resources must be somehow
sharedorbalancedtoreachanequilibriumthatallowsforsustainablepopulations.Thisbalanceisoften
reachedeitherbyverydistinctsegregationinmacrohabitatpreferenceorpreychoice,orbymorespecific
i croh ing d fferencesinmi abitatuse,nest preferences,andtimeofactivity(Ouboter1996).
I would expect a high degree of competition between sympatric apex predators like crocodilians.
Curiously, of an estimated 31 pairs of geographically overlapping species of crocodilians, very few are
found to be in general competition (Ouboter 1996). The apex predator niche divides mostly by habitat
preference; nearly 45% of sympatric crocodile species pairs utilize distinctly different habitat types, i.e.
freshwater vs. coastal water (Ouboter 1996). Coexisting species often further divide their niche by prey
type, usually represented by morphological specialization of head shape, notable between coexisting
muggers Crocodylus palustris and gharials Gavialis gangeticus (Rao and Choudhury 1992) or Crocodylus
porosus and C. johnsoni (Ouboter 1996). There are other ways in which crocodilians will segregate the
nicheofapexpredators,suchasdifferencesintimeofactivity,nestingpreferencesandmicrohabitatuse
(Ouboter 1996). Ouboter (1996) and Soul (2005) suggest that pressures from habitat encroachment
anddestruction(ortheinstigationofconservationtacticswithoutconsiderationofbothspeciespresent)
will increase the competition for shared resources, obstructing the ecological balance of sympatric
populations.
Specificdifferencesinnicheusekeepcoexistingapexpredatorsincompetitiveequilibrium,andtherefore,
directconsequencesexistforthemanipulationofonecoexistingpopulationwithouttheother,especially
sympatricpredators.Thenaturalecologicalinteractionsmustbemaintainedinorderforconservationto
besuccessful(Souletal.2005).
Seekingabalancedstat
Populations occur in a wide range of possible ratios defined first by morphology and resultant
competition, and then by extrinsic factors. They must naturally regulate themselves based on available
resources to ensure survival (St. Amant 1970). With the additionofanother interspecificapex predator,
populationsizesaltertoaccountforthenewspecies.Thelongtermcoexistenceofcrocodilians(Pierceet
al. 2009) proves selfregulatory mechanisms have been successful as the group has not become extinct.
e
Crocodilianshavesimilarecologyanddoaffecteachotherinasharedhabitat(Ouboter1996).
Thedelicatebalance,ensuringsurvivalofbothspecies,betweenpopulations,however,isfurtherstressed
by recent changes to the environment including from human actions toward either positive or negative
goals, such as conservation or habitat destruction. While other factors play a role in the present
abundance of species in different areas, the human impact on limiting habitat and resources has been a
major reason for decline in all species of crocodilians (Aguilera et al. 2008; Ouboter 1996). It becomes
necessary then to assess population ratios between sympatric crocodilians to encourage natural
i
49
regulationtoensuethroughconservationtact cs.
While we expect competition between two coexisting species, a reduction or change in habitat can
significantlythrowoffthebalancebetweencoexistingpopulations.Forsuccessfulcoexistenceinreduced
habitat with shared resources, population sizes can be altered to fit the limitation while optimising self
48
sustainability in both populations present. The ratio of numbers of each species and the distribution of
size classes within each also affects the dynamics of competition and coexistence (Beissinger and
Westphal1998).Inordertodeterminewhatratioallowstwocoexistingpopulationstobeequallyviable,
with minimal impact on each other, I used skull morphospace analysis (Chapter 4) and support those
findingsthroughanexamplestudyofMelanosuchusnigerandCaimancrocodilus.
A skull morphospace analysis to determine niche overlap (Chapter 4) is representative of a balanced
state,asitdoesnotincludehabitatlimitedresources,whichwouldinducecompetition,yetstillgivesan
indication of resource use (Chapter 5). As morphospace overlap disregards habitat and resource
limitations and human influence, it compares to expected population densities in an untouched and
healthy environment. It is also a product of evolution, where coexisting species have, over time,
segregated their niche as noted by different snout shapes, and in turn resource use. For these reasons,
thisamountofoverlapshouldbeaconservationtargetforcoexistingpopulations.
CaseStudy
M. niger and C. crocodilus coexist throughout a large part of their range within much of South America
(Figure 7.1). They maintain similar lifestyle habits, causing competition within the apex predator niche
(DaSilveiraetal.1997;Herron1994).Despitebeingknowntosegregatethisnichebymicrohabitatuse
andsometimedifferences(Herron1994;VanzoliniandGomes1979;Medem1971),theyhaveanimpact
on each other (Magnusson 1982). The degree of competition is dependent on case and often season
specific data. One study found limited food competition during the dry season in Brazil (Marioni et al.
2008) whereas other studies done in the wet season, found that M. niger can affect the ecology of C.
crocodilus (Magnusson 1982; Magnusson and Reblo 1983). They share a similar food source, fish,
however they each supplement this with differing food sources (Ouboter 1996). We can speculate that
there is an ongoing competition leading to a change in one species use of resources, despite reduced
ompetitionduringcertaintimesoftheyear. c
Figure 7.1 Geographic overlap between Caiman crocodilus (red) and Melanosuchus niger (yellow) in South America
e (mapcreat d frominformationcompiledfromCSG2008)
I take as a starting assumption that the morphospace derived from skull measurements of museum
specimens (Chapter 4) reflects the natural condition of these two species whether in sympatry or
occurring alone. As both species are caimans, there was a high percentage of overlap in morphospace
(51%), which this study suggested was also reflective in overlap of niche space. The ratio between M.
nigerandC.crocodiluswithintheinterspecificoverlapwas46%to54%,thatforeveryoneC.crocodilus,
0.852 M. niger could live in sympatry successfully. This was the overlap ratio unhindered by limited
resourcesorhumaninvolvement.
Throughtheapplicationofskullmorphospaceanalysis,thisarticleexaminesthequestion:withincurrent
carrying capacity of a defined area, what population sizes are needed in order to minimize competition
betweenMelanosuchusnigerandCaimancrocodilus,therebyenhancingviabilityofbothpopulations?By
understandingwherealongthepopulationratiogradientspeciescurrentlyfall,wecanenhancemethods
forconservingpopulationsbyaimingforpopulationlevelswhichencouragepassiveinterspecificoverlap.
I also discuss possible strategies for manipulating the situation to push population size to a different
ratio,whichmightbetterconservethespecies.
50
49
Methods
I collected current population data on M. niger and C. crocodilus from literature (Table 7.1) to create an
examplestudy.ThisinformationwasinputintoEquation7.1todeterminetheamountofareaabletobe
used for population expansion. (Equation 7.1 was discussed in Chapter 6.) The ratio acquired from the
skull morphospace analysis acts asa goal equilibrium, in this case 1 C. crocodilus to 0.852M. niger. The
numbersarer h a eassessedinordertoreacht isestim tedequilibriumofpopulationsizes.
Equation 7.1 Equation for determining amount of habitat available for conservation of sympatric
crocodilespecies
whereHA=habitatavailable,A=totalsuitablehabitat,P=populationabundance,HR=homerange,andC=
intraspeci cificgr size ficoverlap,definedasaverageintraspe oup
Table7.1PopulationandecologicalinformationforM.nigerandC.crocodiluswithinasectionoftheMamirau
ustainableDevelopmentReserveinBrazil S
M.niger
612
C. s crocodilu
84
Populationsize(individuals)
Homerange
s/gr
15sq.km
20s km
q.
Overlap(individual oup)
8.5
9
Totalhabitatavailable
*
2810sq.km
P .78
1984)
opulationdensity 696ind./893km
2
=
nformationfromDaSilveiraetal.(1997),OuboterandNanhoe(
onequarteroftheMamirauSustainableDevelopmentReserve
I
*
Step1:Determinedifferenceinnumbersfromcurrentstatetonaturalequilibrium
The previous morphospace analysis found an overlap in niche between the two caiman species to be
byM.n 50%.Ofthis,54%wouldbeusedbyC.crocodilusand46% iger.
ThenumbersinTable7.1showapopulationratioof612M.nigerto84C.crocodilus.Inorderforcurrent
populationstobeequivalenttothenaturalstateequilibrium,Iconsideredthreeoptions(Figure7.2).
1)Thecurrentcombinedpopulationremainsatatotalof696crocodiles.Tomaintainthistotalnumber
andreachequilibrium,theM.nigerpopulationwoulddecreaseto320.2individualsandtheC.crocodilus
increaseto375.8individuals.
2) The larger population is maintained at current size and thus the C. crocodilus population increases to
718individuals.
3) The smaller population is maintained at current abundance and the M. niger population decreases to
8.64individuals. 3
51
50
Figure7.2PopulationabundanceofM.nigerandC.crocodilusfromcurrentpopulationratiothroughthreeoptionsof
populationchange
These options came solely from the population sizes becoming equivalent to the theoretical population
sizes. The coexisting populations can fall along a continuum based on the ratio, within the options
presented. As the changes necessary to create the ideal ratio between species may not be realistic to
naturalormanagedpopulations,otherfactorsmustbeincluded.
Step2:Determineamountofareaavailableforchange
By implementing Equation 7.1 with the numbers from Table 7.1, the area available for conservation
changescanbeestimated.
Basedontheequation,thereisaround1917km
2
ofunusedhabitat.
Step3:Determineamountofchangepossiblewithinconfinesofhabitat
If we assume the carrying capacity is equivalent to the present population density (.78 crocodiles/km
2
),
than the area available for change can hold an estimated 1495.3 crocodiles. This would easily allow for
the second option in Step 1 as the population size of C. crocodilus is only increasing by 634 individuals.
Therewouldstillbespaceforbothpopulationstograduallygrow.
Rarely,however,doesonepopulationstandstillwhileanotheronesoars;populationgrowthrateswould
havetobemonitored.Thetotalamountofspaceavailableis2810km
2
.Thisallowsfor3602.6crocodiles
based on the previous population density. To maintain a 46:54 ratio of M. niger to C. crocodilus, the
estimated population sizes would be 1657.2 to 1954.4, respectively. Since there are already crocodiles
present,theabundancesthenreduceto1045.2M.nigerand1870.4C.crocodilus.Ifthegoalwastoreach
equilibriumwithin10yearsthangrowthrateswouldhavetobemaintainedat17%peryearforM.niger
andover200%peryearforC.crocodilus.
Step4:Determinefocusareasconsiderationsforcreatingchangeinpopulationsize
Inthisexample,conservationeffortsshouldbefocusedonareasofecologicaldifferencetomaximizethe
52
C.crocodiluspopulationwithintheconfinesofthehabitatavailable.
FromOuboter(1996),twomaindifferencesinecologycanbenoted(Table7.2).Thefirstisthedifference
in nesting season; this will reduce competition for nesting ground and hatchling resources (Ouboter
1996). The other difference, which makes habitat more valuable, is the difference in active time. The
limitedhabitat,throughtheecologyofthespecies,hasincreaseditsvalueandsuitabilityformaintaining
multiple populations. Microhabitat is also a nichesegregating factor for these species (Herron 1994,
Magnusson 1985). M. niger prefers aquatic habitat with steep banks and little floating grass while C.
51
crocodilusprefersshalloworgrassyareas(Magnusson1985).Bycreatingshallow,grassyaquatichabitat
intheunusedspace(HA),morepreferentialhabitatisopenedforC.crocodilus,encouragingpopulations
toincrease.
able7.2EcologyinformationforM.nigerandC.crocodilusfromOuboter1996(Table2.1,p.8) T
Foodpreferenceadults
M.
fish,mammals
niger C.crocodilus
fish,crustaceans,terrestrial
invertebrates,snails
Mainhabitat rivers,lakes,inundatedforestand
d grasslan
rivers,creeks,swamps,ponds,
brackishwater
ate Nesttype mound
nks
moundandintermedi
rbanks,marshes Nestinghabitat creekba rive
Nestingseason
imeofactivity
rainy
nocturnal
dry
diurnalandnocturnal T
Discussion
A balanced ratio between sympatric populations is often an unobtainable goal due to expanding human
populations and continually limited resources. However, by indicating a ratio which allows for viable
populationswithminimalcollateralimpact,especiallyincombinationwithanidentifiedlimitedresource
(in this case habitat), I offer a tool through which preemptive planning can lead to more successful
conservation. For two main reasons, this article presents an effective addition to any action plan for
crocodilians.(1)Therehasnotyetbeenanestimateofcrocodilecompetitionwithouttheinputoflimiting
resources. (2) Setting reachable and defined goals within a conservation action plan leads to more
effectiveconservation.
There are some shortcomings to the described method. This study represents an area with a notably
higherabundanceofM.nigercomparedtoC.crocodilus.Withsuchadifferenceinpopulationsize,change
maynotbenecessaryduetolargerpopulationsorbalancedpopulationsinawiderareaunaccountedfor
inthisexample.Becausetheskullmorphospaceanalysiswasbasedonsubadulttoadultspecimens,this
study does not account forsize/age differences within populationsand howthatmay alter the needs or
sizeofthepopulations.
Whileherepresentedisagoalpopulationratioforminimalimpactoneachother,anthropogenicfactors
exists which would increase pressure on both species present and perhaps have altered the acquirable
balance. Human impact is not acknowledged in the equation. Negative interspecific interaction is often
inducedbyhumanintervention(Ouboter1996).Inreality,formyexamplestudyspecies,M.nigeristhe
primary target for hunters, but Da Silveira (1997) says their current populations are sustainable. This
suggests that perhaps the hunting is sustainable, but the sustained population may still be hindering C.
crocodilus populations. Each species may succumb to different pressures, thus why both species need to
beconsideredthroughouttheapplicablerange.
A final shortcoming is that often these species coexist with another two caiman species (Paleosuchus
trigonatus and P. palpebrosus), though on a much wider scale and with further niche segregation. The
addition of these predators would further constrain the M. niger and C. crocodilus populations, but the
53
sameanalysiscanbeexpandedtoincludeallfourspecies.
The method defined in this chapter requires casespecific information, especially for determining focus
areas for creating theoretical equilibrium. If the goal is to maintain population sizes, focus should be on
similarities in ecology and niche use. By focusing on increasing the availability or amount of shared
resources,competitionwouldreduce.Ifpopulationsizesshouldbechanged,thenthefocusshouldbeon
the differences in the ecology and the niche such as nesting or microhabitat preferences. By
52
increasing/expanding, for instance, the amount of habitat preferred by one species, chances for a
population rise in that species increases. Focusing on ecological differences gives more leeway for
populationexpansioninbothspeciesbeforesharedresourcesmustbemanipulated.
Conclusion
Using the skull morphospace overlap of sympatric crocodiles gives an idea of what a natural state for
those species might have been if no factors of recently introduced habitat or resource limitations are
present.Itisnotuncommon,andoftenpreferable,inconservationtointegratetools,suchasthemethods
presented here, by which to optimize the initiatives prior to implementing action plans (Walters and
Hilborn 1978) for betterdirected, more effective action plans. By determining the quantitative
theoretical equilibrium of sympatric crocodilians a goal can be set within action plans and, taking into
consideration casespecific ecology, adds a focus for maximizing success of conservation plans with
minimal impact on coexisting populations. This preemptive action, combining morphometrics and
ecology, is only one way by which management and conservation tactics can be better directed, and the
fieldofpreconservationshouldcontinuetoexpandspecificallywithconcerntoCrocodylia.
Acknowledgements
ZenoWijttenforreviewandcomments.PerranRossfordirectionaladvice.CrocodileSpecialistGroupfor
theStudentResearchAssistanceSchemegrant.
References:
AguileraX,CoronelJS,OberdorffT,VanDammePA(2008)Distributionspatterns,populationstatusand
conservation of Melanosuchus niger and Caiman yacare (Crocodylia, Alligatoridae) in oxbow lakes of the
. g IchiloRiverfloodplain,Bolivia Revista deBiolo aTropical56(2):909929
Beissinger SR, Westphal MI (1998) On the use of demographic models of population viability in
endangeredspeciesmanagement,TheJournalofWildlifeManagement62(3):821841
ableat:http://iucncsg.or/ph1/modules/Crocodilians/ CSG(2008)Crocodilianspecieslist.Avail
species.html[Accessed11March2010]
Da Silveira R, Magnusson WE, Campos Z (1997) Monitoring the distribution, abundance, and breeding
areas of Caiman crocodilus crocodilus and Melanosuchus niger in the Anavilhanas Archipelago, Central
Amazonia,Brazil.JournalofHerpetology31(4):514520
HerronJC(1994)Bodysize,spatialdistribution,andmicrohabitatuseinthecaimans,Melanosuchusniger
f andCaiman crocodilus,inaPeruvianlake.Journalo Herpetology28(4):508513
Magnusson WE (1982) Biological aspects of the conservation of Amazonian crocodiles in Brazil. In:
Crocodiles. Proceedings of the 5
th
Working Meeting of the Crocodile Specialist Group, IUCN/SSC Gland,
Switzerlandpp108116
Magnusson WE (1985) Habitat selection, parasites and injuries in Amazonian crocodilians. Amazonia
9:193204
Magnusson WE, Reblo GH (1983) Brazilian crocodiles: problems of conservation in a multispecies
m system.Zi babweScienceNews17:5657
Medem F (1971) Biological isolation of sympatric species of South American Crocodilia. In: Crocodiles.
Proceedings of the 1
st
Working Meeting of the Crocodile Specialist Group, IUCN Gland. Switzerland, pp
152158
i , Netherlands threepredators.SPBAcademicPubl shingbv,Amsterdamthe
Ouboter PE, Nanhoe LMR (1984) An ecological study of Caiman crocodilus crocodilus in northern
Suriname.MSThesis.Reportno.233,Zol.Lan.Afd.Dieroecologie,Kath.Univ.Nijmegen,theNetherlands
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PierceSE,AngielczykKD,RayfieldEJ(2009)Shapeandmechanicsinthalattosuchian(Crocodylomorpha)
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Soul ME, Estes JA, Miller B, Honnold DL (2005) Strongly interacting species: conservation policy,
managementandethics.BioScience55(2):168176
St.AmantJLS(1970)Determinationofregulationinanimalpopulations.Ecology51(5):823828
Vanzolini PE, Gomes N (1979) Notes on the ecology and growth of Amazonian caimans (Crocodylia,
Alligatoridae).PapisAvulsosdeZoologia,SoPaulo32(317):205216
Walters CJ, Hilborn R (1978) Ecological optimization and adaptive management. Annual Review of
EcologyandSystematics9:157188
55
54
Chapter8
Conclusion
In this thesis, I have tried to describe the relationship between sympatric crocodilians using several
assumptions and a pressing current issue, conservation. Having several interesting data sets, we
combined these to present a picture of crocodile skull morphometrics and its relationship to physical
characteristicswithinaspecies.Withthissupportingwork,wewereabletogivefurtherevidenceofthe
skull being a representation of niche and then further applied this information to the dynamics of
sympatricspeciesnichesegregation.
The root of morphological shape being reflective of ecological characteristics lies in the assumption that
increased physical similarity predicts increased competition for shared resources among crocodilians.
While demonstrated in other species (Schoener 1965; Smith 1990; Aguirre et al. 2002; Adams 2004), it
hasbeenacceptedincrocodilianswithlittlequantitativeevidence. Oncequantitativelyassessed,theuse
ofskullmorphospaceanalysiscanbeappliedtorelationshipsbetweencrocodiliansandusedtoenhance
conservation tactics. The goal of this thesis was to explore the possibility of applying insights derived
fromskullmorphometricstocrocodilianconservation,andapplyingtheseinsightsbeyondthetraditional
rangeofmorphologicalstudies.
Skullmorphometryexplored:theongoingexplorationintospeciesdefiningmorphologicalcharacteristics
Using digital photographic analysis, we explored the crocodile skull, leading to the same difficulties and
conclusions of previous investigators (Pierce et al. 2008). The findings point to the hypothesis that a
difference in the skull shape should exist which can be used as a character for species identification. In
thisthesis,asuiteofcarefulskullmeasurementsdoesprovideadiagnosticshapeparameterthatclearly
differentiates different species of crocodilian and allows inferences about their function and ecological
niche.However,furtherdefinitionofspeciesspecificmorphologicalcharacteristicsmighttaketheformof
complex algorithms. This fundamental research could offer a way to indentify species when genetic
analysis tools are unavailable or too costly for execution. When this measurement or algorithm is
successfullyidentified,wecangiveanonthegroundapproachtospeciesrecognitionforlocalgameand
wildlifeprotectors.
Interspecificskullscompared:definingtherelationshipbetweensympatricspecies
Icomparedtheskullsofsympatriccrocodiliansusingamorphospaceanalysis.Themorphospaceoverlap
reflectednicheoverlapinwildpopulations.Iverifiedthisthroughtheallometryofthebodywiththeskull
relating to habitat and nesting preferences. The morphospace analysis offered a unique perspective on
niche segregation in multispecies environments. In many cases, there are unknown factors affecting
crocodilian communities or some ecological or physiological aspects as yet unexplored (notably in the
PhilippinecrocodileC.mindorensis).Incaseslikethis,conservationistscandeduceageneralideaofwhat
the estimated overlap between sympatric species could be within restrictedarea environments. In this
way,thestudyshowsthatskullmorphospaceanalysisisreflectiveofrealizedniche,atleastinpart,and
canbeusedtounderstandrelationshipsbetweensympatricspecies.
Integrationintoaconservationplan
The use of morphospace overlap ratios as a balanced state offers a goal for defining conservation
expectations. Through this, the oftenunderestimated impact of sympatry can be accounted for within
conservationandmanagementtactics,therebyreducingnegativeimpactonsympatricspecies.Thestudy
presentsanapplicationofskullmorphologytocrocodileconservationandmanagementthroughtheuse
of an equation based on habitat as a limiting factor. The application can be to large or smallscale
populations or areas, but when focused on smaller populations or areas, must account for populations
bordering the study area. There is a limitation in that the study does not focus on the protection of the
habitat itself. Habitat degradation, destruction, and loss are the greatest threat to crocodilian survival
worldwide(Ross1998;Thorbjarnarson1999).Theapplicationpresentedshowshowtoworkwithinthe
confinesofsuitablehabitatbutnothowtoexpandthem,otherthanacknowledgingexpectedincreaseof
valueasdeterminedbyecologicaldifferencesofthesympatricspecies.
56
55
Furtherstudiesandtranscendinglessons
Thephotographicmethodsdevelopedinthisworkcouldbeappliedtootherorganismsthatarewell
representedinmuseumcollectionstoconductsimilarmorphospacenicheestimationanalysisand
informconservation.
Anotherinterestingapplicationofthisstudywouldbewithinhybridspecies.Hybridsarebecomingmore
and more common both in captive and in wild situations (FitzSimmons et al. 2002; Weaver et al. 2008;
CedeoVsquez et al. 2008). If there is a notable change in skull shape among hybrids, then it is worth
studying whether that change makes them better able to coexist or to survive. The skull shape analysis
alone could lend insights to several other interesting characteristics within the hybrids themselves, like
c ldi plasticity,inheritability,andphysiologi a fference.
A combined morphospace analysis of a multitude of physical characteristics along with the skull may
betterdefinenichedivision.
Therelationshipsbetweenextinctspecieswouldbeaworthwhileuseofthisstudyaswell.Evolutionhas
played a role in the ecological relationships that currently exist (Ross 2004). From research into extinct
species,onecouldinferreasonsforcurrentrelationshipsandwhyspecieswhichliveinhighcompetition
still coexist. If ancestral relationships were less competitive, i.e. their morphological overlap was less,
thancurrentrelationships,thiscouldperhapsexplainthecontinuedcoexistenceasonespeciesevolvedto
becomemoredominantwithintheapexpredatorniche.Thisinformationcanbeusedtodetermineniche
overlapwithinextinctspeciesandlendinsightintocurrentsympatricstatuses.
Finalstatements
Crocodile populations affect each other. We have shown this and shown how it can be accounted for in
conservation efforts. While of proven help in crocodilian conservation, the same problems exist
throughoutecologybecauseallspeciescompete.Thisistheparadigmofecology,evolutionandspeciation
because populations always affect each other. This study is applicable to a broad range of populations
competing within niche space. In other reptiles, the skull would be examined, although it is conceivable that
characteristics in other species would be examined in a similar fashion. However, this study is aimed at
sympatricspeciesofcrocodilians,andthustheconclusionsderivedheremaynotapplytospeciesgroups,
wherepopulationgroupswouldbemorecomplicated,thisbeingamoresimplifiedversion.
Morphological studies have shown their worth in a variety of fields within crocodilians. This thesis has
nowextendedthat(throughintegrationwithmodelingschemes)tothemostnecessaryandpressingfield
of extant crocodilians: conservation. The endangered status of crocodilians (IUCN 2010), the ever
encroaching human populations, and the declining habitat availability, warrant research into different
options for conservation directives. This thesis, with its ratio analysis and carryingcapacity estimates,
canalsobeavaluableasset,toassessmentofhabitatavailabilityandhumanencroachment,bufferzones,
park management, release programs and even husbandry techniques. Along with addition of such
applications, this thesis has given credence to the longaccepted hypothesis of skull shape determining
competitionbetweencoexistingspecies.
References:
damsDC(2004)CharacterdisplacementviaaggressiveinterferenceinAppalachiansalamanders. A
Ecology85(10):26642670
AguirreLF,HerrelA,vanDammeR,MatthysenE(2002)Ecomorphologicalanalysisoftrophicniche
partitioninginatropicalsavannahbatcommunity.ProceedingoftheRoyalSociety:BiologicalSciences
269(1497):12711278
CedeoVsquez JR, Rodriguez D, Calm S, Ross JP, Densmore LD, Thorbjarnarson JB (2008)
Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan peninsula: I. evidence
frommitochondrialDNAandmorphology.309A(10):661673
57
56
FitzSimmons NN, Buchan JC, Lam PV, Polet G, Hung TT, Thang NQ, Gratten J (2002) Identification of
purebred Crocodylus siamensis for reintroduction in Vietnam. Journal of Experimental Zoology (Mol Dev
Evol)294:373381
IUCN (2010). IUCN Red List of Threatened Species. Version 2010.1. <www.iucnredlist.org>. Accessed on
22March2010
nd
SpecialistGroupIUCN,Gland,SwitzerlandandCambridge,UK
Eds):CrocodilianBiologyandEvolution.SurreyBeattyandSons,ChippingNorton,NSW,Australia,pp1 (
2
choenerTW(1965)Theevolutionofbillsizedifferencesamongsympatriccongenericspeciesofbirds. S
Evolution19(2):189213
SmithTB(1990)ResourceusebybillmorphsofanAfricanfinch:evidenceforintraspecificcompetition.
Ecology71(4):12461257

Weaver JP, Rodriguez D, VenegasAnaya M, CedeoVsquez JR, Forstner MRJ, Densmore III LD (2008)
Genetic characterization of captive Cuban crocodiles (Crocodylus rhombifer) and evidence of
hybridization with the American crocodile (Crocodylus acutus). Journal of Experimental Zoology 309A
(10):649660
58
57
Appendices
"Howdiditgetsolatesosoon?Itsnightbeforeafternoon.DecemberisherebeforeitsJune.My
howthetimehasflewn.Howdiditgetsolate
59
goodness
sosoon?
Dr.Seuss
58
AppendixI
Listof159m
Taxon
Alligatoridae
useumspecimensused
60
SpecimenNo. Museum
Alligatormississippiensis 402 ZoologicalMuseumAmsterdam
Alligatormississippiensis 413
c
ZoologicalMuseumAmsterdam
Alligatormississippiensis 1698 RoyalBelgianInstituteofNaturalSciences
Alligatormississippiensis 169 RoyalBelgianInstituteofNaturalSciences
ianInstituteofNaturalSciences
Alligatormississippiensis 169, RoyalBelg
Alligatormississippiensis 172 RoyalBelg
Naturalis
442
27
Naturalis
Alligatormississippiensis 19861 ParisMNHN
Alligatormississippiensis 19191 ParisMNHN
Alligatormississippiensis 37166 Senckenberg
SenckenbergNHM
Alligatormississippiensis 59421 SenckenbergNHM
uteofNaturalSciences
Alligatormississippiensis 151219 SenckenbergNHM
Alligatorsinensis 3487 RoyalBelgianInstit
Alligatorsinensis 40071
5
SenckenbergNHM
Alligatorsinensis 4968 SenckenbergNHM
Alligatorsinensis 3219a SenckenbergNHM
lMuseumAmsterdam
Caimancrocodilus 412 Zoologica
Caimancrocodilus 12630 RoyalBelg
Caimancrocodilus 37541 Naturalis
Caimancrocodilus 37638 Naturalis
Caimancrocodilus 40173 SenckenbergNHM
Caimanlatirostris 12629 RoyalBelgianInstituteofNaturalSciences
InstituteofNaturalSciences
Caimanlatirostris 13522
44
RoyalBelgian
Caimanlatirostris 25793 RoyalBelgianInstit
Caimanlatirostris 19879 ParisMNHN
Caimanlatirostris 28193 SenckenbergNHM
Caimanlatirostris 43925
SenckenbergNHM
Caimanyacare 13521a RoyalBelgian
Caimanyacare 13521b RoyalBelgianInstit
Caimanyacare A5305 ParisMNHN
Caimanyacare 28182 SenckenbergNHM
NHM
NHM
Caimanyacare 30107 Senckenberg
Caimanyacare 55763
2
7
Senckenberg
Melanosuchusniger 190011
ParisMNHN
0
ParisMNHN
Melanosuchusniger 19867 ParisMNHN
Melanosuchusniger A530A ParisMNHN
Melanosuchusniger 28179 SenckenbergNHM
28182
35100
SenckenbergNHM
SenckenbergNHM
SenckenbergNHM
Melanosuchusniger
Melanosuchusniger
59
61
Paleosuchuspalpebrosus 37550 Naturalis
Paleosuchuspalpebrosus 197706 ParisMNHN
NHM
NHM
Paleosuchuspalpebrosus 40064 Senckenberg
Paleosuchuspalpebrosus 43957
5
uffetau
Senckenberg
Paleosuchustrigonatus 19770 ParisMHNN
Paleosuchustrigonatus 1978B ParisMNHN
Paleosuchustrigonatus 36730
50399
SenckenbergNHM
SenckenbergNHM Paleosuchust
Paleosuchust
Crocodylidae
rigonatus
rigonatus 51662 SenckenbergNHM
Crocodylusacutus 2446
SenckenbergNHM
Crocodylusacutus 28412 SenckenbergNHM
Crocodylusacutus 60848 SenckenbergNHM
Crocodyluscataphractus
Crocodyluscataphractus
4990 RoyalBelgianInstituteofNaturalSciences
Crocodyluscataphractus 4997 RoyalBelgianInstituteofNaturalSciences
Crocodyluscataphractus 4998 RoyalBelgianInstit
Crocodyluscataphractus 5000 RoyalBelgianInstit
Crocodyluscataphractus 28138 SenckenbergNHM
Crocodyluscataphractus 54119 SenckenbergNHM
NHM
Crocodyluscataphractus 83021 Senckenberg
Crocodylusintermedius 13235
92
36
RoyalBelgian
Crocodylusintermedius 19301 ParisMNHN
Crocodylusintermedius 19442 ParisMNHN
Crocodylusintermedius A5310 ParisMNHN
Crocodylusintermedius 28139 SenckenbergNHM
ergNHM Crocodylusjohnsoni 54425 Senckenb
Crocodylusjohnsoni 54426 SenckenbergNHM
Crocodylusmindorensis 37505
9
Naturalis
Crocodylusmoreletii
Crocodylusmoreleti
2816 SenckenbergNHM
i
Crocodylusniloticus
56317 SenckenbergNHM
Crocodylusniloticus
Crocodylusniloticus
411 ZoologicalMuseumAmsterdam
Crocodylusniloticus
Crocodylusniloticus
Crocodylusniloticus
Crocodylusniloticus
5018 RoyalBelgian
Crocodylusniloticus
5019 RoyalBelgian
1930176
8
ParisMNHN
19866 ParisMNHN
Crocodylusniloticus 19914480
02
ParisMNHN
Crocodylusniloticus A5307 ParisMNHN
Crocodylusniloticus Cr.561 ParisMNHN
Crocodylusniloticus 28158
SenckenbergNHM
Crocodylusniloticus 18162 SenckenbergNHM
Crocodylusniloticus 29081 SenckenbergNHM
ergNHM
ergNHM
Crocodylusniloticus 4018 Senckenb
Crocodylusniloticus 47827 Senckenb
Crocodylusnovaeguineae 21821 Naturalis
Crocodylusnovaeguineae 28150 SenckenbergNHM
ergNHM
NHM
Crocodylusnovaeguineae 60030 Senckenb
Crocodylusnovaeguineae 60031
37522
1944229
Senckenberg
Naturalis
ParisMNHN
Crocodyluspalustris
Crocodyluspalustris
60
Crocodyluspalustris 28168 SenckenbergNHM
Crocodylusporosus 11907 ZoologicalMuseumAmsterdam
Crocodylusporosus 13069
70
120
ZoologicalMuseumAmsterdam
Crocodylusporosus 161 RoyalBelg
Crocodylusporosus 161| RoyalBelg
Crocodylusporosus 37510 Naturalis
Crocodylusporosus 37640 Naturalis
Crocodylusporosus 23190 SenckenbergNHM
Crocodylusrhombifer 12613 RoyalBelgianInstit
NHM Crocodylusrhombifer 37081
6
Senckenberg
Crocodylusrhombifer 37169
2
7
SenckenbergNHM
Crocodylussiamensis 1980
6
ParisMNHN
Crocodylussiamensis 281 SenckenbergNHM
Osteolaemustetraspis 409 ZoologicalMuseumAmsterdam
Osteolaemustetraspis ZoologicalMuseumAmsterdam
Osteolaemustetraspis 10518
5
RoyalBelgianInstituteofNaturalSciences
Osteolaemustetraspis 105 3 RoyalBelgianInstituteofNaturalSciences
Osteolaemustetraspis 16616 RoyalBelgian
Osteolaemustetraspis 130|
0
488
RoyalBelgian
Osteolaemustetraspis 19523 ParisMNHN
Osteolaemustetraspis 19914
72
15
ParisMNHN
Osteolaemustetraspis 281 SenckenbergNHM
Osteolaemustetraspis 401 SenckenbergNHM
lMuseumAmsterdam
Tomistomaschlegelii Zoologica
Tomistomaschlegelii 154 RoyalBelg
Tomistomaschlegelii 35446 Naturalis
Tomistomaschlegelii 35447
8134
Naturalis
enckenbergNHM
NHM
Tomistoma
Tomistoma
Gavialidae
schlegelii 2 S
schlegelii 28135 Senckenberg
49
50
Gavialisgangeticus 19442 ParisMNHN

N Gavialisgangeticus 19442 ParisMNH
Gavialisgangeticus A5132 ParisMNHN
Gavialisgangeticus 37641 Naturalis
Gavialisgangeticus 28133
37951
49529
SenckenbergNHM
SenckenbergNHM
SenckenbergNHM
G
G
avialisgangeticus
avialisgangeticus
62
61
AppendixII
ListofCrocodylusspecimensfromDavaoCrocodilePark
Specimen
. No
Species
Specimen
. No
Species
Specimen
o. N
Species
6.0.47 C.porosus 6.0.23
C.porosus
1.15
C.mindorensis
6.01.19
C.porosus
6.0.12
C.porosus
1.39
C.mindorensis
3.0.2
C.porosus
6.12.24
C.porosus
1.0.46
C.mindorensis
6.01.29
C.porosus
1.0.26
C.mindorensis
1.12.1
1.3.38
C.mindorensis
6.0.67
C.porosus
13.0.4
C.mindorensis
C.mindorensis
6.01.12
C.porosus
1.0.8
C.mindorensis

6.1.17
C.porosus
1.0.1
C.mindorensis

7.34.16
C.porosus
1.0.48
C.mindorensis

7.34.13
C.porosus
1.0.16
C.mindorensis

7.0.38
9
C.porosus
1.0.57
8
C.mindorensis

7.28.34
C.porosus
1.0.17
C.mindorensis

6.1.39
C.porosus
1.0.9
C.mindorensis

6.0.49
C.porosus
1.0.4
C.mindorensis

6.1.12
C.porosus
1.0.3
C.mindorensis

6.1.15
C.porosus
1.0.56
C.mindorensis

6.0.68
C.porosus
1.0.67
C.mindorensis

6.1.47
C.porosus
1.0.24
C.mindorensis

6.0.89
C.porosus
1.0.3
C.mindorensis

7.29.46
C.porosus
1.0.25
C.mindorensis

6.1.49
C.porosus
1.0.36
3
C.mindorensis

6.0.29
C.porosus
1.0.1
C.mindorensis

6.0.57
C.porosus
1.05
C.mindorensis

7.29.78
C.porosus
1.0.23
C.mindorensis

6.0.39
C.porosus
1.0.27
C.mindorensis

6.1.18
C.porosus
1.0.2
C.mindorensis

6.0.19
6.0.17
C.porosus
1.49
1.34
C.mindorensis

C.porosus C.mindorensis

63
62
AppendixIII
Klins1212asanindicatorofsizeinCrocodylia
+
Abstract
The attempt to identify the best measurement of size in crocodilians is an ongoing research, constantly
revisited with fresh ideas. The skull is most frequently used as it is often what remains in museum
collections and is easier to measure than mass or total body length. Klin (1933) proposed a set of
measurements for examining the crocodilian skull. I examined one of these, termed Klin 1212 and
located at the width of the skull at the anterior side of the medial postorbital bar suture, compared to
other straight line skull measurements, as a measurement for size in crocodilians based on four criteria
deemedimportantforassessingascientificallyviablemeasurement:(1)lowvariability,(2)correlationto
bodysize,(3)functionalimportanceand(4)repeatability.Basedonthesefourcriteria,Klin1212serves
as a suitable measurement location for crocodilian size, presenting less variation than previously used
measurementsoftotalwidthandlength.
Introduction
Thesearchforthebiggestcrocodileisafrequentendeavornotonlyforspectaclebutalsoforthesakeof
science and evolutionary understanding Whitaker and Whitaker 2008). However, there is often
confusionoverthebestmeasurementlocationfordeterminingsize(RossandPearcy2009).Anaccurate
andeasilyidentifiablemeasurementwouldbebetterabletoanswerwhichcrocodileisthebiggestandto
predict the size of an animal from its skull. Klin (1933) proposed a series of crocodilian skull
measurements.Oneofthese,termedKlin1212,isthewidthoftheskullmeasuredattheanteriorpoint
ofthepostorbitalbarmedialsuture.IexaminedKlins1212asameasurementforsizeincrocodilians
basedonthefollowingcriteriaderivedfromanumberofsources(HallandPortier1994;McIntosh1955;
Pierce2008;Verdade2000):(1)lowvariability,(2)correlationwithbodysize,(3)functionalimportance,
and(4)repeatability.
Sincecrocodileskullsaremoreoftenthannottheonlypreservedelementoftheskeleton,measurements
onskullsarefrequentlyusedtoestimatethesizeofindividuals.Theskullisallometricallyrelatedtobody
size and canthus be used in determining the physical size of a specimen rather than mass or total body
length (Greer 1974; Woodward et al. 1995). However, the criterion for size must encompass the least
variable aspect to be applicable within and across species (McIntosh 1955). Total skull length has
previouslybeenconsideredtobetheindependentvariableindicatingsize(Radinsky1981;Simpson,etal.
1960).Therehavebeendebatesonthisassumptionaswidestpointofthecraniumhasalsoproventobe
anotablevariable(MonteiroandSoares1997).Mostcommonlyusedhasbeentheratiobetweenthetwo
skullwidthandskulllength(Busbey1995,Verdade2000).
Thesecommonlyusedmeasurementsofskulllengthandwidthareoftensusceptibletonotablevariation
within the ontogenetic process and change outside of this process. For example, hatchling skull shape,
specificallyintherostrum,isdifferentfromthatoftheadultofthesamespecies(Dodson1975;Halland
Portier 1994; Verdade 2000). Outside of the ontogenetic process other changes occur. Depending on
physical environmental conditions and stress factors, skull shape as described by total length and total
width, can alter dramatically, as commonly seen in captive populations (Hutton 1987). Growth can be
extremely variable within species (Hall and Portier 1994; Hutton 1987). This variability can be larger
when comparing healthy vs. unhealthy and captive vs. wild (Black and Loveridge 1975; Coulson et al.
1973;JoanenandMcNease1974;WhitakerandWhitaker1977).Whiletraditionalmeasurementsoftotal
length and total width can be informative of how large an individual is, the disparity between size of
individuals,causedbyontogeneticfactors,andaveragesizeofthespeciescanreduceapplicationamong
comparativemorphometricstudies.
Methods
Measurements were made from the widest part of the mandible at the level of the anterior side of the
artothesamepointontheoppositesideoftheskull(Figure1c,d;Klin
sthisareaisidentifiedasthespacebetweentheearflapandt ebackof
64
medialsutureofthepostorbitalb
1212).Onskincoveredspecimen
+
PearcyA(2010)Klin1212asanindicatorofsizeincrocodilians.HerpetologicalReview41(4):445447
63
theeye.Thedistancefrommidlineatthiswidth(Figure1g)tothetipofthesnout(Figure1a)isKlins
123.
Onlyonetraditionalwidthmeasurement,cranialwidth(CW),wasexamined.Thatisthewidthofthejaw
atKlin1(1933)asdefinedbythewidestpointonthequadratojugalbone(Figure1:e*,f*).Totallength
of skull (TSL) is from posterior margin of the parietal bone (Fig. 1b) along the midline to the anterior
tremityofthepremaxillary(Klins63)(Figure1a).Allmeasurementsweretakenincentimeters. ex
Figure1Measurementstakenfromcrocodilianskulls;ab:totalskulllength,cd:Klin1212,ef:totalwidthofskull,
ag:Klin123.Asterisksmarktraditionalmeasurement.
Datawerecollectedfrommuseumspecimens(N=152)ofall23speciesofextantcrocodilians.Fromthese
specimens, the four aforementioned measurements were taken. Juveniles and noticeably deformed
specimens were not used if possible. A separate data set was used, where whole specimens, not only
skulls, were examined for comparison of measurements to the total body. These measurements of total
body length (TBL) and snoutvent length (SVL) were collected on 21 wild Osteolaemus tetraspis by a
crocodileexpeditionthroughoutcentralAfrica(Zoer2010).Aropewasusedtotakethemeasurementon
thecrocodileandthenmeasuredalongatapemeasure.TBLwastakenonthedorsalsurface,whileSVL
wasmeasuredalongtheventralsurface.
IcomparedKlins1212 measurementstoCWandTSLusingPearsoncorrelationanalysestheKlin12
withSPSS16.0.OnewayANOVAswereruntotestforthedifferencebetweenratios.Standarddeviations
andttest(Dinov2005)werethencalculatedwithineachmeasurementtypeforeachspeciesinMicrosoft
Excel2008.AprincipalcomponentsanalysiswasusedtobetterdefinethedifferencebetweentheKalin
1212ratioandthetraditionalratioastheyrelatetospeciesdifferentiation.
Results
Correlation analyses of TSL and CW, and TSL and Klin 1212 for all species show positive correlations
betweentheKlin12measurementratio(R=0.875)andthetraditionalmeasurementratio(R=0.908).
TheratioofCWtoTSLdidnotsignificantlydifferfromtheratioofKlin1212toKlin123(ANOVA:F=
0.54,df=1,p=0.46).
Standard deviations within measurements were examined (Table 1). Standard deviations were lower
within Klin measurements than within traditional measurement. A ttest found Klin1212 to be
significantlydifferentthanCW(t=5.1,df=20,p<0.001)andthesamebetweenKlin123andTSL(t=
4.320,df=20,p<0.001).
A principal components analysis between the Klin 12 ratio and the traditional ratio between species
found that 97.34% of the variation is accounted for in principal component 1. Case loadings show that
C1isdrivenbytheKlin12ratio(0.82)ratherthanthetraditionalratio(0.58)toseparatebyspecies. P
65
64
Table1.Samplesize,sizerangeandstandarddeviations asurementsbyspecies. withinme
via Standardde tions
Species N RangeCW(cm) Klin1212 CW Klin123 TSL
A.mississippiensis 13 16.1030.28 3.67 5.04 6.48 7.31
A.sinensis 4 9.6015.10 2.24 2.33 3.02 3.61
C.acutus 3
19.9035.72 5.93 8.26 14.16 15.63

C.cataphractus 8 20.0726.86 2.05 2.31 4.36 4.76
C.crocodilus 12 12.3716.55 0.99 1.21 2.03 2.19

C.intermedius 9 20.0035.50
.2014.10
4.44
99
47
5.75
34
57
8.73
26
22
10.08
69
85
C.johnsoni 2 12 0. 1. 2. 2.
C.latirostris 9 12.3023.65 3. 4. 3. 3.
C.mindorensis 1
C.moreletii 2 13.0827.40
C.niloticus 17 20.9037.40 5.15 6.41 9.11 10.47
C.novaeguineae 3
14.0022.10 3.08 4.06 4.85 5.78

C.palustris 7 15.6034.84 5.09 6.99 8.39 14.4
C.porosus 12 28.5043.94 5.08 5.98 5.63 6.27
C.rhombifer 3 10.6923.70 5.50 6.87 4.97 7.52
C.siamensis 2 15.2223.10 4.26 5.57 7.89 9.89
C.yacare 6 13.5019.70
2.14 2.56 2.46 3.21

G.gangeticus 7
20.3529.55 3.69 3.66 7.54 7.57

M.niger 8 18.8033.91 4.23 5.56 6.46 7.56
O.tetraspis 10 8.5011.28 0.75 0.92 0.92 1.23
P.palpebrosus 3
5
6
9.7015.49
8.2015.75
19.6041.97
2.25
2.84
7.95
3.00
3.51
12.02
3.65
5.17
12.77
4.69
6.20
14.08
P
T
.trigonatus
.schlegelii
Datagatheredon21OsteolaemustetraspisrevealedthestandarddeviationoftheratiobetweenKlin12
12 and total body length (SD=0.175) was lower than the standard deviation of CW to body length ratio
(SD=0.192).Withinthesamedataset,thestandarddeviationofwidthatKlin12tosnouttoventlength
(SVL)(SD=0.0138)waslowerthanthatofcranialwidthtoSVL(SD=0.282).Acorrelationanalysisshows
slightlyhighercorrelationbetweenSVLandKlin1212(R=0.977)thanSVLtoCW(R=0.958).
Discussion
Although measurement locations in morphology can be changed to suit the purpose of a study, a good
generalizedmeasurementforindicationofsizeincrocodiliansisusefulinavarietyoffields.Fourcriteria
wereusedtoinvestigatetheusabilityoftheKlin12measurementsasameasurementofsize,findingit
tobeofvalueoverothermeasurements.
Lowvariability
The best size measurement is the least variable one (McIntosh 1955). The Klin 1212 measurements
havealowerstandarddeviationwithinspeciesthandothemeasurementsoftotalwidthandtotallength.
The lower deviations within species supports the hypothesis that the Klin 1212 and Klin 123
measurements are less susceptible to growth outside of the ontogenetic process and maintain less
66
variationthanothermethods.
Klin 1212 also occurs in an area, near the orbits, of reduced allometric growth coefficient, (Verdade
2000;Wu2006)whichmeansthatthegrowthrateofthisareaisreducedcomparedtosnoutlengthand
widthatthebackofthejaw,whichaccountsforthelowerdeviation.Thereducedgrowthofthisportion
of the skull at later stages of crocodile development is also reported in a study of C. novaeguineae (Hall
and Portier 1994). Hall and Portier (1994) did not specify the exact position of Klin 1212, and I
compared their measurements of orbital width and postorbital cranial table width to snoutvent length.
Hutton (1987) used a measurement on C. niloticus from the point anterior to the orbits to the tip of the
snout, finding that it grows in relative proportion to head width (Hutton 1987). This is the closest
measurementcomparabletoKlin123.Astheareaaroundtheorbitsislesspronetogrowthextremes,
it represents a more accurate figure for skeletal size. This can be especially important in captive
65
populations where growth responds to temperature, population density and food (Blake and Loveridge
1975; Coulsonet al. 1973; Joanen and McNease 1974; Whitaker and Whitaker 1977), thereby creatinga
comparabledatabase.
Forskincoveredspecimens,thelocationofKlin1212isalsoanareaofreducedsofttissue,whichcould
preventdiscrepanciesinmeasurementsbasedonthethicknessofsofttissue.
Correlationwithbodysize
When compared to body length and snoutvent length, Klin 1212 has a lower standard deviation than
CW.ThisshowsthatKlin1212isaviablemeasurementofsizeevenfortotalbodylengthinO.tetraspis.
AsO.tetraspisisthesmallestcrocodile,thelowerstandarddeviationofKlin1212maybedueinpartto
thecrocodilessmallsize.However,thepreviousanalysisshowsthesamepositivityforKlin12inskull
size for all species. The direct proportions between the skull and body of crocodilians (Chentanezet al.
1983; Hutton 1987; Verdade 2000) backs the assumption that Klin 1212 is a viable measurement
relatabletototalbodysizeinspeciesotherthanO.tetraspis.
Change in one part will result in the restructuring of the entire skull (Monteiro et al. 1997). We would,
therefore, expect a similarity between the Kalin 12 measurements and CW and TSL and their respective
ratios, as they are related measurements of length and width, which is a verifiable proportion within
crocodilians(Chentanezetal.1983;HallandPortier1994).
Functionalimportance
While functional importance is not always a necessity for determining a measurement point, it can be
beneficial for application to ecology and functional morphology. The area of the skull surrounding the
orbitshasareducedsusceptibilitytoabnormalgrowth,anditisaphysicallystrongpointontheskull.In
battle, crocodilians have been known to bash heads (Webb and Manolis 1989) with the point of contact
often near Klin 12. In spite of the dangers to either side of the focal point this rarely seems to cause
damage. Due to the closing of the secondary palate, the crocodilian rostrum is much stronger near the
orbits than expected. According to Busbey (1995) this does lead to less tension from torsional loads
associated withfeeding behaviours. Posteriorand anterior toKlin12 the skull is also weaker.The jaw
hingeisapointofweakness,andwherethesnoutelongates,andinmanyspeciesthins,itismorelikelyto
fractureorbreak.
Repeatability
The postorbital bar offers an area easily identifiable on skulls. On skincovered specimens there is a
minimum margin of error as the distance between the earflap and the eye is small. Although the widest
partoftheskullseemseasiertoidentifythenKlin12,inmanyskullsfromcollections,theboneisoften
chippedorbrokenatthewidestpart,whichisapparentlymostsusceptibletodamage.Thewidestpartof
theskullcanalsobeopentointerpretationasanywherebetweenthebackofthequadrojuglebonetothe
widestpartofthatbone.
Conclusion
Basedonthecriteriausedhere,theKlin1212measurementsprovedtobeaslightlybetteradaptation
to the traditional width measurement at Klin 1. It offers an easily identifiable area, which is less
susceptible to growth due to environmental factors, and the low amount of soft tissue in this area also
reducesthebiasalreadyfoundinskincoveredvs.cleanspecimens.Klin1212measurementsmayalso
bebettermeasurementswithincaptivepopulations,wheremalnourishmentandstressfulconditionscan
leadtoabnormalgrowth.Klin1212isalsoofphysiologicalimportancebeingoneofthestrongerareas
of the crocodilian skull. The use of Klin 12 could benefit comparative anatomy, evolutionary, and
ecologicalstudiesofcrocodiliansbypresentingameasurementmeetingprovencriteriaforusability.
67
Acknowledgements
FranklinD.Rossforthemeasurementandthechallengetoproveatheory.ZenoWijttenforassistancein
datacollectionandmanuscriptrevisions.RolandZoer,RogierdeBoer,andJeroenKoorevaarforsharing
datafromtheirAfricaexpedition.Dr.FransWitteandNicoleOrtegaforcomments.RoyalBelgianInstitute
66
of Natural Sciences, Forschungsinstitut und Naturmuseum Senckenberg, Naturalis, Zoological Museum
Amsterdam,ParisMNHNforaccesstotheircrocodilianskullcollections.
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in individuals. Herpetological Monographs 8:203-225
Hutton J M (1987) Growth and feeding ecology of the Nile crocodile Crocodylus niloticus at Ngezi, Zimbabwe.
A J ournal of nimal Ecology 56(1):25-38
Joanen T, McNease L (1974) Propagation of immature American alligators in controlled environmental
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Microsoft (2008). Excel 12.0. Office for Mac 2008
Monteiro L, Soares M (1997) Allometric analysis of the ontogenetic variation and evolution of the skull in
, 1 Caiman Spix 825 (Crocodylia: Alligatoridae). Herpetologica 53(1):62-69
Monteiro L, Cavalcanti M, Sommer III H (1997) Comparative ontogenetic shape change in the skull of
Caimanspecies(Crocodylia:Alligatoridae).JournalofMorphology231:5362
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Ross FD, Pearcy A (2009) Maximum width of adult cranium. Crocodile Specialist Group Newsletter 28(4):15
Simpson GC, Roe A, Lewontin RC (1960) Quantitative Zoology. Harcourt Brace, New York
SPSS, Inc. (2008). SPSS 16 for Mac OS X. SPSS Inc., Chicago
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Verdade LM (2000) Regression equations between body and head measurements in the broad snouted caiman
(Caiman latirostris). Revista Brasiliera de Biologia. 60(3):469-482
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68
ppendixIV:Skullshapesandgeographicoverlapofselectedsympatricspecies
+
A
Figure1AustralianandIndiansympatricspeciesshowingskullshape,skulloverlapandgeographicoverlap
+
/
AllgeographicoverlapfromCSG(2008)Crocodilianspecieslist.Availableat:http:
modules/Crocodilians/species.html[Accessed29March2010]
//iucncsg.or/ph1
70
69
F
o
igure2TwosympatricspeciesfromSouthAmericaandthethreespeciesfoundinAfricashowingskullshape,skull
verlap,andgeographicoverlap
71
70
Figure3SympatricspeciesofCubaincludingtheintroducedC.crocodilussowingskullshape,skulloverlapand
geographicoverlap
72
71
Summary
Each species of crocodile has its own distinct head shape with its own welladapted capacities for
movement,force, strength,and inturndiet and habitat preferences suiting their niche. Differentspecies
of crocodilians with overlapping or matching natural ranges (sympatric species) show increased
(interspecific)competitionwithsimilarityinheadshape.Usingvariousskullmeasurementsofallextant
i adsh crocodilianspecies,Itriedtoquantify and descr be similarityanddissimilarityinhe ape.
I use this information to ascertain the level of competition, and thus impact, the presence of one
crocodilianspecieswouldhaveonanother.Thisisconsideredforboththeareaofdirecteffect(syntopic
zone) and as a ripple effect throughout the area of shared habitat (sympatric range). As a result it is
possibletopredictratiosinwhichthecoexistingspeciesmustremain(naturalstateequilibriums)sothat
bothpopulationsaresuccessful.Iappliedthefoundinterspecificcompetitionrelationshipstofiveknown
sympatricspeciespairsandcorroboratedthismethodwithacomparisontoexistingpopulationstudies.
I suggest the derived ratios as guidelines for conservation and management decisions within multi
species habitats, where probable impact of one apex predator on another is often unknown, difficult to
deduct from ecological studies or underestimated. The ratios are integrated into a study addressing the
mostimportantfactorofpopulationdecline:habitatloss.Howeversincethewayinwhichcrocodilesuse
the available habitat is a big factor in itself, I also share insights into speciesspecific focus areas for
onservation,suchasnesting,foodavailability,baskingspace,etc. c
73
72
Samenvatting
+
Elke krokodillensoort heeft zijn eigen specifieke vorm kop met ieder aanpassingen en eigenschappen, perfect
voor specifieke bewegingen, kracht en sterkte. Op hun beurt hebben deze eigenschappen invloed op voeding,
habitatvoorkeuren en dus hun leefgebied en niche. Verschillende soorten krokodilachtigen hebben vaak
overlappende of gelijke natuurlijke leefgebieden. Deze ovelappende of sympatrische soorten vertonen vaak
hogere (interspecifieke) concurrentie naarmate kopvormen meer overeen komen. Doormiddel van het meten van
schedels van alle bestaande soorten krokodilachtigen, heb ik geprobeerd de overeenkomst en verschil in
kopvorm kwantitatief te beschrijven.

De kwantitatieve informatie gebruik ik om competitieniveaus vast te stellen; de invloed van aanwezigheid van
de ene krokodillensoort op de andere. Ik beschouw hierbij zowel directe effecten, in de syntopische zone, als
indirecte effecten in de gedeelde habitat of sympatrische range. Vervolgens is het mogelijk om voorspellingen te
doen met betrekking tot populatie ratios of natuurlijke equilibria. I heb deze methode getest op vijf paar
sympatrische krokodillen soorten en de resultaten vergeleken met werkelijke populatienummers uit andere
studies.

In veel gevallen wordt bescherming van krokodillen soorten bemoeilijkt doordat de invloed van soorten op
elkaar onbekend is, lastig is af te leiden of onderschat wordt. In deze gevallen kunnen de hier beschreven ratios
dienen als hulpmiddel. Ik integreer de ratios in een studie naar de belangrijkste factor voor populatie daling:
verlies van habitat. Het gebruik van een beschikbare habitat door krokodillen is echter een belangrijke factor op
zich. Daarom deel ik ook inzichten in gerelateerde aandachtsgebieden voor de instandhouding van de soort,
zoals nestgedrag, de beschikbaarheid

van voedsel en mogelijkheden tot regulatie van lichaamstemperatuur.
74
+
translatedbyZenoWijtten
73
Resumen
+
Lacabezadelcocodrilotieneunaformadiferenteynicasegnsuespecie,adaptandoperfectamentesus
capacidadesalmovimientoylafuerza,ytransformandosudietaysuspreferenciasdelhbitatasunicho
ecolgico. Las diferentes especies de cocodrilos cuyas cabezas tienen formas similares y cuyos hbitats
coincidenosesuperponenmuestranunaumentoenlaluchaporlosrecursos.Usandovariasmedidasen
crneosdetodaslasespeciesexistentesdecocodrilos,heintentadocuantificarydescubrirlassimilitudes
f ylasdiferenciasenlas ormasdesuscabezas.
Uso esta informacin para comprobar el nivel de competicin y, de esta manera, el impacto que la
presenciadeunaespeciepuedetenersobreotra.Estorepercuteenelreadelhbitatcompartido,siendo
tanto un efecto directo como un efecto onda. Como resultado es posible predecir los ratios en donde
deben permanecer las especies que cohabitan de manera que las dos poblaciones tengan xito en la
subsistencia. He aplicado los ratios encontrados a cinco parejas de especies cohabitantes y he
corroboradoestemtodocomparndoloconlosestudiosdepoblacinexistentes.
Yo sugiero los ratios encontradoscomo gua para la conservacin yel manejo dedecisiones encuantoa
los hbitats de especies donde el posible impacto del predador de rango ms alto sobre otro de rango
inferioresamenudodesconocido,subestimadoodifcildededucirenlosestudiosecolgicos.Losratios
estnintegradosenunestudiodirigidoalaprdidadelhbitat,loculconformaelfactormsimportante
deldeclivedelapoblacin.Sinembargo,yaquelamaneraenqueloscocodrilosusanelhbitatdisponible
esungranfactorensmismo,tambinpropongoideasfocalizadasencadaespecieespecficatantopara
lasreasdeconservacincomoparalaanidacin,ladisponibilidaddelacomida,lugaresparacalentarse
alsol,etc.
75
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translatedbyVeronicaTerrienteGarcia
74
Acknowledgements
percent. ImeantwhatIsaidandIsaidwhatImeant.Anelephant'sfaithful,onehundred
Dr.Seuss
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correctedwithmuchpushingandshovingandwinkingandnudging.Itwassolelyabouttheacquisitionof
a degree and knowledge, and those willing to share, discuss, chat, commend, condemn, and ultimately,
achieveagoal.Icouldnothavebeensuccessfulwithoutyou:
Zeno, where do I begin? Without your discussions, constant support, and distractions from the
frustrations, this would have been a dead end street. You have tackled the impossible with me and
provedittobeotherwise.Yourinputwasinvaluableandyourchallengesformidable.Ilearnsomething
fromyoueveryday,andthataloneisworththankingyoufor.Thankyouforbeingmybestfriend,silver
liningandmyrock,seeingmethroughthisseeminglycatastrophicjourney.
MomandDad,thiswasthelastchapterinmyeducation.Thankyouforgivingyoursupportformyzany
adventures and farfetched plans. I suppose they will continue to come but perhaps with more subtly. I
loveyou.BrodidyoueverthinkyouwouldbeteachingyoursisterstatisticsoverSkype?Thanksforthe
help.Nene,thankyouforourmorningchats,yoursupport,andunderstanding.Tomyfamilyandfriends
Statesside, and indeedother placestoo,thank you for your continued support with regard tomy often
selfishlifestyle.
Philippines: Kuya Willie, thank you for taking care of me and for listening to, analyzing, and suggesting
solutionstomyinnumerableproblems.ThankyoutoAndyRoss,VicMercado,andSonnyDizonforgiving
measecondchanceandbelievingthatIcouldbesuccessful.ThankstothestaffofDavaoCrocodilePark
fortheirassistancewithhandlingcrocodilesandforlettingmeenjoytheotherreptiles,thestaffofDavao
Wild Water for showing me the lighter side of life, and the Forum for Philippine Crocodile Conservation
fortheirfunding.
FrankRossandDonnaRichoux,thanksforhelpingmeinsomanyways.Thanksformakingmethinkand
presenting challenging views on crocodiles, thanks for the thorough proofreading and comments, and
thanksforthemultipledinners.
Museums:GuntherKoehlerandhisgroupofSenckenbergNaturalHistoryMuseum,HielkePraagmanand
Ronald Vonk of Zoological Museum of Amsterdam, Georges Lenglet of the Royal Belgian Institute of
Natural Sciences, Roger Bour of the Reptiles and Amphibian Department and the Comparative Anatomy
DepartmentofParisMNHN,andRonalddeRuiterandPimArtzenofNaturalis
ThankyoutoallotherswhohavehelpedmegetthisfarProf.MikeRichardson,Dr.PerranRoss,Denyse
Snelder, Jacques van Alphen, Frans de Witte, Liesbeth den Hollander, Roland Zoer, Ashly Eikelberg,
HerbertPrins,VeronicaTerrienteGarcia
Toanyonewhofeelsleftout,thankyoutoo.
Thankyouallforpassingonknowledgeofanyandallkinds,forthisiswhatIaimtodo.
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PublicationList
earcy A (in progress) From skull shape to conservation: a case study of M. niger and C. crocodilus. P
(Chapter7ofthisthesis)
earcy A (in progress). Assessing carrying capacity for sympatric crocodilian populations. (Chapter 6 of P
thisthesis)
earcy A, Wijtten Z (in progress) Physical characteristics defining niche advantages in Philippine P
crocodiles.(basedonChapter5ofthisthesis)
earcy A. (in review) Defining niche segregation between sympatric crocodilians using skull
s
P
morphospaceanalysi .Herpetologica(Chapter4ofthisthesis)
earcy A., Wijtten Z (in revision) A morphometric analysis of crocodilian skull shapes. Herpetological P
Journal(Chapter3ofthisthesis)
earcy A, Wijtten Z (2010) Suggestions for photographing crocodile skulls for scientific purpose. P
HerpetologicalReview41(4):445447(Chapter2ofthisthesis)
earcyA (2010) Klin 1212 as an indicatorofsize. HerpetologicalReview 41(4): 434437 (Appendix III P
ofthisthesis)
earcy A, Wijtten Z (2010) Application of skull morphology to conservation of sympatric crocodilians. P

20
th
WorkingMeetingoftheCrocodileSpecialistGroup,Manaus,Brazil,1217September2010
earcyA,WijttenZ(2010)Ecologicalimplicationsofskullmorphologyinsympatricapexpredators.11 P
n
th
ternationalConferenceofArchaezoology,Paris,France,2328August2010,p199 I
PearcyA(inpress)KeelbackTropidonophismairiipreypreference.AustralianZoologist
(inpro re PearcyA g ss)Assessmentofbenefitsanddisadvantagestowetlandweedmanagement
ossFD,PearcyA(2009)Maximumwidthofanadultcranium.CrocodileSpecialistGroupNewsletter28 R
(4):15
oer R (2010) Catching crocodiles in the heart of darkness. Pearcy, ed. Uitgeverij Boekscout.nl, Soest, Z
77
Netherlands
ZoerR,vanHoevenW,PearcyA(inprogress)ThepersistenceofthebushmeatmarketsincentralAfrican
countries
76
Curriculumvitae
hanYou."
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BornonSeptember26
th
1985inNashville,Tennessee,USA,Iwasalittlecountrygirlwithbigaspirations.
Following my schooling in 2003, I moved to Florida to pursue my Bachelors degree where reptiles run
rampant and the sun always shines. I finished early and graduated with Honors in 2005 with a double
majorinBiologyandMarineSciencefromtheUniversityofTampa.InmytimeinTampa,Ididmultiple
research projects including a study on Anolis populations on spoil islands and their reaction to invasive
floraspecies,methodsfordeterminingmercurylevelsinfishtissue,andpopulationdistributionofwater
snakes in a wetland near urban development. I also did an internship in the Herps and Aquatics
Department at Lowry Park Zoo. From Florida, I had a 6month hiatus working in Death Valley National
Park in California. I then moved to Australia to pursue my Masters degree in Tropical Biology at James
CookUniversityinTownsville,Queensland.Mystudyfocusedontheherpetofaunainaninvadedwetland
including predatorprey relationships and affects of weed management. This also included a wet season
study, something rarely attempted in tropical North Queensland. The research was funded by a
substantial grant from the Burdekin Dry Tropics NRM. I again finished early (2007), completing a two
year degree in 16 months. Before I had received my degree, I had already moved to the Philippines to
begin work on the endangered Philippine crocodile Crocodylus mindorensis. I consulted on a social
conservation project in North Luzon, in order to assist with the ecological projects. I transferred to
Mindanao to consult on and do research with crocodile farms. I was given a grant by the Forum for
Philippine Crocodile Conservation to do preliminary studies in Agusan marsh, searching for crocodile
populations. After working in Mindanao, I returned to the Netherlands to continue my PhD in 2009. A
partofthedatacollectedinmytimeinthePhilippineswasusedinmyPhDstudies.MyPhDworkwillbe
presentedattheInternationalConferenceinArchaeozoologyinParisinAugust2010andalsoatthe20
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CrocodileSpecialistGroupWorkingMeetinginManausinSeptember2010.
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ImplicationsofSkullShapefortheEcologyand

Linking Conservation and Skull Morphology in the Study of Sympatric Crocodilians:

Figure 2.1 showsthedorsalviewofthecranium.Thereddotshowsthecenter point along the midline of the skull

uneven, we leveled the skul

Terborgh J , Estes J A, Paquet P, Ralls K, Boyd-Heger D, Miller BJ (1999)InMESoul,JTerborgh(Eds):

Gavialisgangeticus 19442 ParisMNHN

19.9035.72 5.93 8.26 14.16 15.63

C.crocodilus 12 12.3716.55 0.99 1.21 2.03 2.19

14.0022.10 3.08 4.06 4.85 5.78

2.14 2.56 2.46 3.21

20.3529.55 3.69 3.66 7.54 7.57

earcy A, Wijtten Z (2010) Application of skull morphology to conservation of sympatric crocodilians. P

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