relationships among foraging variables, phylogeny
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Herpetologica, 61(3), 2005, 250259 2005 by The Herpetologists League, Inc.
RELATIONSHIPS AMONG FORAGING VARIABLES, PHYLOGENY,AND FORAGING MODES, WITH NEW DATA FOR
NINE NORTH AMERICAN LIZARD SPECIES
WILLIAM E. COOPER, JR.1,4, LAURIE J. VITT 2, JANALEE P. CALDWELL2, AND STANLEY F. FOX3
1Department of Biology, Indiana University-Purdue University at Fort Wayne,Fort Wayne, IN 46805, USA
2Sam Noble Oklahoma Museum of Natural History and Department of Zoology,University of Oklahoma, Norman, OK 73072, USA
3Department of Zoology, Oklahoma State University, Stillwater, OK 74078, USA
ABSTRACT: Complete characterization of lizard foraging behaviors may require information about aspectsrarely measured. Most studies record only number of movements per minute (MPM) and/or percent of timemoving (PTM), but lizards differ markedly in average speed (AS) and speed while moving (MS) duringforaging and in proportion of attacks initiated after detecting prey while the lizard is moving (PAM). We
present data on these variables for nine lizard species and on foraging speed for several others, permitting firstassessments of relationships between speed, PAM, and both phylogeny and foraging mode; examination of theeffect of body length on foraging speed; and correlative analyses of relationships between foraging variables.Although sprint speed may increase with body size, foraging speed did not, presumably for two reasons.Because search speed is much lower than sprint speed, as is speed of movement between ambush sites,searching efficiency and stamina may be more important determinants of foraging speed than is sprint speed.Second, the body size range was small, allowing the possibility that foraging speed may vary with body lengthover the much larger size range between the smallest and largest species worldwide. Nevertheless, a largemajority of lizard species are in the size range tested, suggesting that body length may not strongly affectforaging speed except when extremely short or long species are included in comparative analyses. High PAM,high AS, and low MS were characteristic of autarchoglossans and active foragers, whereas low PAM, low ASand high MS were exhibited by iguanians and ambush foragers. In independent species analyses, significantcorrelations were observed between several pairs of foraging variables. In analyses using phylogeneticallyindependent contrasts, the only significant finding was a strong positive correlation between PAM and PTM.
Although these findings suggest that foraging speed, MPM, and either PTM or PAM may provide independentmeasures of foraging activity needed to adequately describe interspecific variation, this conclusion is tentativedue to the small sample size of limited taxonomic breadth.
Key words: Foraging behavior; Foraging mode; Foraging speed; Lizard; Squamata
LIZARD foraging behavior has been inten-sively investigated since the early 1980s, inlarge part to test predictions made by Huey andPianka (1981) and others (e.g., Huey andBennett, 1986; Regal, 1978; Schoener, 1971;
Stamps, 1977; Vitt and Congdon, 1978) aboutconsequences of ambush foraging and activeforaging for several aspects of lizard ecology,behavior, sensory capacities, and morphologyand relationships between foraging modes,physiology and locomotor performance. Thesestudies have been very fruitful, leading to theforaging mode paradigm that seeks to explainmuch of the evolutionary and ecological di-
versity of lizards (Vitt et al., 2003).Although numerous correlates of foraging
mode have been discovered, the existence of
the distinct foraging modes has become con-troversial. Some investigators maintain thatlizard foraging behavior exhibits sufficientcontinuous variation that ambush and activeforaging modes are inadequate to characterize
it (Perry, 1999; Pietruszka, 1986). Others havecontinued to recognize the existence of dis-crete foraging modes either based on bimodal-ity of the distribution of continuous foraging
variables (McLaughlin, 1989), the occurrenceof two distinct groupings in discriminantanalyses (Butler, in press), or convenience ofstatistical analysis for testing hypotheses aboutfactors related to foraging behavior (Cooper,1995, 1997).
It has been clear for over 40 years that
foraging behavior differs greatly among majorlizard taxa and is very stable within some largetaxa (Cooper, 1994a,b; Evans, 1961; Perry,1999). As more data have become available for4 CORRESPONDENCE: e-mail, [email protected]
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an ever-increasing diversity of lizard families,much continuous variation has been discov-ered within and among taxa, leading to theconclusion that two modes are inadequate toexpress all of the variation (Perry, 1999, inpress). However, data remain unavailable forseveral important lizard families and the
number of species sampled even in largefamilies remains small. More data are neededto assess the extent to which foraging behaviormay vary continuously among species or maybe divided into categories corresponding toseparate modes, each characterized by internalcontinuous variation.
For a large majority of species for whichforaging behavior has been quantified, data arerestricted to number of movement bouts perminute and/or percent time spent moving.
These are important features of searching forprey, but other important information isneeded to characterize foraging behavior morefully. Huey and Pianka (1981) reported averagespeed during focal observations and speed
while moving during foraging, but informationon foraging speeds has rarely been publishedsince their paper (see Cooper and Whiting,1999 for an exception). One reason for therarity of speed data may be that Huey andPianka (1981) noted that differences in forag-
ing speeds might be attributable to differencesin body size, making them difficult to interpretand perhaps requiring adjustment for inter-specific differences in body size.
Because ambush and active foraging modesare methods of searching for prey, Cooper and
Whiting (1999) proposed that the proportion ofattacks on prey initiated after discovering theprey while moving (PAM) could be a superiorindex of foraging mode. They and Cooper et al.(2001) presented data on this variable for
limited numbers of African lacertids and forNorth American representatives of severalfamilies, but more data are needed to assessthe utility of PAM and relationships betweenPAM and other foraging variables.
We report new data on all variables dis-cussed above for nine species of NorthAmerican lizards representing four familiesand present foraging speeds for additionalspecies for which movements per minute(MPM), percent time moving (PTM), and
PAM were reported previously (Cooper et al.,2001). We provide a first test of the hypothesisthat foraging speed varies with body length. Bycombining our data with previously publisheddata, we assess for the first time possibledifferences in foraging speeds and the attack-based index between major lizard taxa andforaging modes. We examine for the first timecorrelations among all foraging variables.
MATERIAL AND METHODS
Lizard species, samples sizes and duration ofobservations for species observed in 2004 arepresented in Table 1. Sceloporus arenicolous
TABLE 1.Sample sizes (n), duration of observations (minutes), number of movements per minute (MPM), and percenttime moving (PTM) sizes for 9 species of North American lizards.
Family Species n Minutes
MPM PTM
x SE Range x SE Range
Phrynosomatidae
Sceloporus arenicolous 5 32.4 0.80 0.42 0.200.24 1.4 0.7 0.34.0S. merriami 11 109.9 0.24 0.06 0.000.60 0.9 0.3 0.03.7S. poinsettii 12 104.2 0.08 0.03 0.000.30 0.2 0.1 0.00.8S. sleveni 16 144.0 0.24 0.05 0.000.53 0.4 0.1 0.00.9S. undulatus 15 142.2 0.31 0.10 0.001.49 1.0 0.4 0.05.3
Polychrotidae
Anolis sagrei 22 209.1 0.25 0.06 0.000.90 0.5 0.0 0.00.2
Tropiduridae
Leiocephalus carinatus 24 230.0 0.20 0.05 0.001.00 0.5 0.1 0.02.0
Teiidae
Aspidoscelis exsanguis 12 103.7 0.75 0.08 0.401.30 82.4 2.9 67.199.0A. tessellata 9 41.9 1.01 0.09 0.591.45 88.6 3.2 71.896.8
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were observed on 24 May in the MescaleroSands in Chaves County, New Mexico; S.
merriami on 30 April to 2 May and S. poinsettiion 12 May at Black Gap Wildlife Manage-
ment Area in Brewster County, Texas; S.sleveni on 19 May and Aspidoscelis (formerlyCnemidophorus) exsanguis on 918 May in theChiricahua Mountains of Cochise County,Arizona (Herb Martyr area in CoronadoNational Forest, on the grounds of theAmerican Museum of Natural Historys South-
west Research Station, and in the ChiricahuaNational Monument); S. undulatus and A.
tesselata on 23 May in Eddy County, NewMexico; and Anolis sagrei and Leiocephaluscarinatus on 1926 June in Palm Beach, PalmBeach County, Florida. All lizards observed
were adults except eight A. exsanguis. Becausesex differences in MPM and PTM were notdetected in studies of other North Americanspecies (Cooper et al., 2001) using similar orlarger sample sizes, sexes were not recorded.
An observer walked slowly through eacharea to sight lizards for focal observations usingunaided vision and searching with binocularsto detect lizards at greater distances to reducepossible disturbance. Upon detecting a lizard,
an observer stopped moving immediately, alsoto minimize disturbance. The distance be-tween observer and lizards during observa-tions was greater than 5 m in all but a few casesnoted below. Many individuals of the largerambush-foraging species, S. poinsettii and L.carinatus, were observed at distances greaterthan 30 m. Aspidoscelis sp. typically wereobserved at relatively short distances as theyforaged actively, moving into and through
vegetation and other objects that obscured
them from view at greater distances. Theirmovement sometimes required that the ob-server move to keep them in view, especiallyfor individuals that moved relatively longdistances. Fortunately, by moving slowly only
while a lizard is moving and maintaininga minimum distance of five meters betweenlizard and observer while the lizard is moving,it is possible to observe normal foraging by
Aspidoscelis sp. with minimal disturbance(Anderson, 1993; Cooper et al., 2001). As in
previous studies of Aspidoscelis (Anderson,1993; Cooper et al., 2001), some individualsof A. exsanguis and A. tesselata (formerly A.
grahami) changed direction and approached
the immobile observer, appearing to be un-aware of his presence.
Each focal observation lasted 10 min whenpossible. However, focal observations were
sometimes shorter (Table 1), with a minimumof 1.5 min for all but one species becauselizards sometimes moved to locations wherethey could not be observed. Shorter intervals(68 and 72 s) were accepted for two individualsof S. arenicolous because the sample size forthis species was very small. Foraging data wererecorded on microcassette tapes only forindividuals that did not appear to have beendisturbed. To minimize possible effects ofdisturbance to the lizard that could not bereadily discerned, an observer waited 2 minafter detecting a lizard and stopping beforebeginning a focal observation. To ensure thatdata points were independent, individuals
were observed only once. To accomplish this,each area was sampled only once and beforemoving to a new location. For each focalobservation, the species, locality, date, time,and food-related behaviors were noted. Thebehavioral data recorded were time spentmoving (to the nearest second), time spentimmobile, distances moved (to the nearest
0.1 m), feeding attempts, and whether feedingattempts were made after detecting prey whilethe lizard was immobile or while it wassearching actively. Lizards that are not walkingor running often move specific body parts suchas the head or tail. Only translational move-ments, i.e., ones to new locations, wereincluded in estimates of time spent movingand distance moved. Thus, postural changesand movements of specific body parts bylizards not moving the entire body to a new
location did not contribute to estimates of timemoving or distance moved.Several foraging variables were calculated
from the movement and attack data. PTM andMPM (e.g., Cooper et al., 1997, 2001; Hueyand Pianka, 1981; Perry, 1999, in press), themost widely used indices of lizard foragingbehavior, were calculated. Ambush foragershave lower PTM than active foragers, butMPM is more variable within foraging modes.The other foraging movement variables were
average speed (AS), i.e., distance moveddivided by observation time in seconds, andspeed while moving (MS), which is distancedivided by time moving.
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The final foraging variable was PAM, calcu-lated as number of attacks on prey discovered
while moving divided by total attacks by bothmoving and immobile lizards. Movements byambushers needed to attack prey detected by
lizards while immobile must be excludedbecause they are part of the attack rather thansearch for prey. PAM provides a more directmeasure of the outcomes of sit-and-wait versusactive search than PTM or MPM and requiresno information about time spent moving,number of movements, or speed. PAM cansupplement these latter variables and eventu-ally may provide an excellent comparativemeasure of search by ambush versus whileactive. It also might help to assess relationships
among the other measures of foraging activity.However, PAM data are available for fewerspecies than other foraging variables becausedata collection is much more time-consumingfor PAM than the other variables. PAM isespecially difficult to estimate for ambushforagers having low feeding rates.
Environmental conditions may affect lizardactivity strongly. In particular, heliothermicspecies spend more time basking and less for-aging at lower temperatures; at high temper-
atures, time spent in thermoregulatory coolingby shuttling between sunny and shaded sites orresting in shade increases with temperature(e.g., Vitt et al., 1993 for A. deppii). To ensure
that estimates of foraging activity are compa-rable for between species, it is necessary tomake observations under conditions that favornormal foraging activity. Species observed inthe present study are all diurnal, and all had
free access to sunlit and shaded sites, permit-ting normal thermoregulation. Focal observa-tions were made only on sunny days whenmorning basking had been completed andlizards were active. The data represent foragingactivity by lizards at or close to preferred bodytemperatures for each species because bodytemperatures are maintained within a narrowrange while heliothermic species are active.Preferred body temperatures vary amongspecies, but foraging is usually conducted by
each species in its own range of preferredbody temperature.In comparative analyses involving species
not studied in 2004, published data were usedfor all variables for five lacertid species (Cooperand Whiting, 1999) and for PAM, PTM andMPM for a crotaphytid, six phrynosomatids,a skink, and four teiids (Cooper et al., 2001).Previously unpublished AS and MS for speciesin Cooper et al. (2001) are presented in Table2. Maximum speed may vary with body length,
but whether foraging speed does is unknown.To determine whether speed variables shouldbe adjusted for body length, we conductedregressions of AS and MS on snoutvent length
TABLE 2.Average speed (m/s), speed while moving (m/s), and sample sizes for North American lizard species studied byCooper et al. (2001).
Average speed Moving speed
Family Species n x SE Range n x SE Range
Crotaphytidae
Crotaphytus collaris 39 0.003 0.001 0.0000.036 14 0.689 0.168 0.0502.286
Phrynosomatidae
Cophosaurus texanus 14 0.002 0.011 0.0000.153 13 0.612 0.191 0.0722.316Holbrookia propinqua 14 0.006 0.002 0.0000.027 12 0.477 0.132 0.1071.676Sceloporus clarkii 20 0.000 0.001 0.0000.021 14 0.457 0.142 0.0041.829S. jarrovii 46 0.003 0.001 0.0000.016 37 0.351 0.057 0.0211.625S. virgatus 19 0.003 0.001 0.0000.015 19 0.186 0.027 0.0250.432Urosaurus ornatus 20 0.005 0.001 0.0000.027 24 0.225 0.035 0.0250.596
Scincidae
Eumeces laticeps 25 0.030 0.004 0.0030.082 25 0.042 0.006 0.0080.134
TeiidaeAspidoscelis deppii 39 0.030 0.003 0.0020.072 39 0.049 0.004 0.0130.107A. sexlineata 12 0.063 0.009 0.0330.113 12 0.092 0.008 0.0430.145A. sonorae 9 0.050 0.009 0.0280.076 9 0.051 0.009 0.0310.077A. uniparens 29 0.058 0.006 0.0180.158 29 0.070 0.007 0.0200.197
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(SVL) for 19 species in the phylogeny pre-sented below. SVLs were obtained from Vittet al. (1993), Branch (1998), Conant and Collins(1998), and Stebbins (2003). Differences inPAM between iguanian and scleroglossanlizards were examined for significance usinga Mann-WhitneyU-test for limited data avail-able from the present study, Cooper et al.(2001) for several families of American lizards,
and Cooper and Whiting (1999) for five speciesof African lacertids. Estimates of PAM basedon less than four observations for a singlespecies were excluded. For Mann-WhitneyU-tests of phylogenetic differences in speed
variables, present data were combined withdata on African lacertids for which n ! 5 fromCooper and Whiting (1999). Phylogeneticdifferences in MPM and PTM were not testedhere because they have been examined byPerry (1999) for a much wider range of species.
Relationships among PAM, MPM, PTM,and foraging speeds were examined usingsimple linear regression and correlation (Zar,1996) as well as the method of independentcontrasts (Felsenstein, 1985). The traditionalnonphylogentetic (tips) approach was usefulfor indicating the extent to which two variablesapparently indicate the same degree of forag-ing activity, and independent contrasts wereneeded to determine whether correlated evo-lution has occurred between variables. For
correlations using independent contrasts, weused phylogenies from Reeder (1995), Reederand Wiens (1996), Wiens and Reeder (1997),and Flores-Villela et al. (2000) for phrynoso-
matids; Schulte et al. (1998) for iguanians;Wright (1992) and Reeder et al. (2002) forteiids; Fu (2000) for lacertids; and Estes et al.(1988) for autarchoglossans. Independent con-trasts were computed using COMPARE 4.6.
Branch lengths in Garland (1994) wereused, but were unavailable for some branches
whose lengths were estimated by assumingearly divergence among families. The phy-
logeny and branch lengths used were:(((Leiocephalus carinatus:151, Crotaphytuscollaris:151):10, ((Cophosuarus texanus:3, Hol-
brookia propinqua:3):62, (Urosaurus orna-tus:26.3, ((Sceloporus jarrovii:1, S. clarkii:1,S. virgatus:2):24.3):38.7):96):10, (Eumeceslaticeps:155, ((Pedioplanis namaquensis:2, P.
undata:2):6, (Heliobolus lugubris:5, (Merolesknoxii:2, M. ctenodactylus:2):3):3):138,(Aspidoscelis deppii:6, (A. sexlineata:3, (A.exsanguis:2, (A. uniparens:1, A. sonorae:1)
:1):1):3):140):9):16):1.All tests of significance were two-tailed witha 5 0.05. Although unadjusted P values arepresented in results, reported significance hasbeen verified by sequential Bonferroni adjust-ment (Wright, 1992) for the number of regres-sions. Data in the text are reported as x 6 SE.
RESULTS
2004 Data
Although MPM values were variable, PTM,average speed, and speed while moving weresimilar among all species except the two teiids(Tables 1, 3). The four Sceloporus spp., the
TABLE 3.Average speed (m/s), speed while moving (m/s), and sample sizes for nine species of American lizards.
Average speed Moving speed
Family Species n x SE Range n x SE Range
Phrynosomatidae
Sceloporus arenicolous 5 0.002 0.001 0.0000.008 5 0.165 0.037 0.0150.262S. merriami 11 0.001 0.000 0.0000.004 8 0.226 0.086 0.0550.806S. poinsettii 11 0.001 0.000 0.0000.007 5 0.301 0.091 0.1270.635S. sleveni 16 0.002 0.001 0.0000.005 12 0.441 0.079 0.1521.075S. undulatus 15 0.005 0.002 0.0000.023 12 0.390 0.057 0.0760.740
Polychrotidae
Anolis sagrei 15 0.001 0.000 0.0000.004 14 0.259 0.026 0.1190.521
Tropiduridae
Leiocephalus carinatus 24 0.003 0.000 0.0000.011 18 0.543 0.082 0.0501.130
Teiidae
Aspidoscelis exsanguis 12 0.029 0.005 0.0090.047 12 0.032 0.005 0.0120.075
A. tesselata 12 0.030 0.003 0.0190.045 9 0.035 0.005 0.0200.063
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polychrotid, and the tropidurid exhibitedmovement patterns typical of ambush foragers.MPM was low (,0.33) in most of theseiguanians, the only exception being S. arenic-
olous for which sample size was small. PTMwas ,1.5% in all iguanians, indicating thatthey spent a large majority of the timeimmobile, hunting by ambush. Combined withprevious data for other of Sceloporus and
Anolis, present data confirm low PTM in thesetaxa. For eight species of Sceloporus, PTM is1.36 6 0.66 with range 0.185.84. For 19species of Anolis (sensu lato), PTM is 1.63 60.47 (range 0.087.20). The two teiids aretypical active foragers. In both species of
Aspidoscelis, MPM was substantially higherthan in iguanians other than S. arenicolous.Their PTM values were typical for the genusand much higher than those of iguanians.
PAM data were obtained only for fourspecies and were limited in all cases. Scelopo-rus merriami attacked once, Anolis sagreitwice, and L. carinatus four times from am-bush. Because none of these species was ob-served to attack during active search, PAM 50.00 for each species. Aspidoscelis exsanguisattacked eight times, all as a result of discov-
ering prey during active search, givingPAM 5 1.00.
Foraging speeds differed dramatically be-tween iguanians and teiids. Iguanians had AS 50.002 6 0.001 m/s (range 0.0010.005), farlower than AS for the two teiids, which were0.030 6 0.001 m/s, with range 0.0290.030 m/s.Iguanians, however, had much faster speedsduring movements, MS 5 0.332 6 0.0500 m/s
with range 0.1650.543 m/s, compared to theteiids, for which speed while foraging was only
MS 5 0.034 6 0.002 m/s with range 0.0320.035 m/s.
Phylogenetic Differences in ForagingSpeed and PAM
For the 19 species used in regressions andphylogenetic analyses below, foraging speeds
were not significantly correlated with bodylength (AS 5 0.19 SVL 0.05; F 5 0.64; df51, 17; P . 0.43; MS 5 0.14 SVL 0.13; F 50.36; df5 1, 17; P . 0.56). Therefore, foraging
speeds were not adjusted for differences inbody size in the following tests.Average speed of the seven iguanian species
observed in 2004 was far less than that of the
two teiid and five African lacertid species,which was AS 5 0.036 6 0.007 m/s (range0.0070.059) even though one of the lacertids(Meroles knoxii) is an ambush forager. The
average speed of the lacertids and teiids wassignificantly greater than that of the iguanians(U 5 0.0; n 5 7, 7; P , 0.001 each). Averagespeed of the six species of active foragers(0.041 6 0.006 m/s) was significantly greaterthan that of the eight species of ambushforagers (0.002 6 0.001 m/s; U 5 0.0; P ,0.002). Speed while moving was significantlygreater for seven iguanians than for the teiidsand lacertids, for which MS 5 0.091 6 0.034m/s, range 0.0320.159 m/s (U5 0.0; n 5 7, 7;P , 0.001). Moving speed of eight ambushforagers (0.311 6 0.110) was significantlygreater than that of the six active foragers(0.079 6 0.032; U5 0.0; n 5 6, 8; P , 0.002).
Adding present data, PAM estimates arenow available for eight iguanian, one scincid,five teiid and five lacertid species. PAM 5 0.00for all of the iguanians, and one lacertid that isan ambush forager. For all of the autarcho-glossans, PAM 5 0.83 6 0.10, with range 0.001.00. For all of the actively foraging species (allbut the one species of the autarchoglossans),
PAM was 0.92 6 0.07, with range 0.331.0.PAM was significantly lower for representa-tives of the iguanian families Phrynosomatidae,Tropiduridae, and Crotaphytidae than forrepresentatives of the autarchoglossan familiesLacertidae, Teiidae, and Scincidae (U5 4; n 58, 11; P , 0.001). It was significantly lower forambush foragers than active foragers (U 50.00; n 5 9, 10; P , 0.001).
Relationships between Foraging Variables
In independent species analyses, PAM wasstrongly and significantly related to PTM(PTM 5 0.97 PAM 2.09; F 5 231.84; df 51, 17; P , 1 3 106), but was not significantlyrelated to MPM (F 5 3.78; df 5 1, 17; P ,0.069). MPM and PTM were not significantlyrelated to each other (F 5 2.66; df5 1, 17; P ,0.13). Average speed and moving speedexhibited a negative linear relationship to eachother having the equation AS 5 0.63 MS 0.05 (F 5 11.14; df 5 1, 17; P , 0.004). Both
speeds were significantly related to PAM,average speed positively (AS 5 0.87 PAM 0.01; F 5 54.09; df 5 1, 17; P 5 2.0 3 106)and moving speed negatively (MS 5 0.78
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PAM 0.40; F 5 25.84; df5 1, 17; P 5 9.2 3105). Average speed had a positive, butnonsignificant, linear relationship with MPM(AS 5 0.44 MPM0.02; F 5 4.14; df5 1, 17;
P5
0.058) and a highly significant relationshipwith PTM (AS 5 0.87 PTM0.01; F 5 50.90;df 5 1, 17; P 5 2.0 3 106). Moving speedhad a negative linear relationship with bothMPM (MS 5 0.53 MPM 0.37; F 5 6.70;df 5 1, 17; P , 0.019, marginally nonsignifi-cant after Bonferroni adjustment) and PTM(MS 5 0.78 PTM0.40; F 5 26.58; df5 1, 17;P 5 7.9 3 105).
Most of these relationships were not signif-icant in the phylogenetic analyses using in-dependent contrasts (Table 4). PAM and PTM
were the only variables that were significantlycorrelated (r 5 0.84; df 5 1, 17; P , 0.001).The correlation between PAM and averagespeed was suggestive, but not significant afterBonferroni adjustment (r 5 0.50; df 5 1, 17;P , 0.032). No other correlations approachedsignificance in the independent contrastsanalyses.
DISCUSSION
Foraging Differences between Clades andForaging Modes
All iguanians in this study exhibited thelow PTM characteristic of ambush foragers,
whereas the two species ofAspidoscelis exhib-ited much higher PTM values typical for activeforagers. MPM is more variable than PTM
within foraging modes among lizards becausesome ambush foragers move briefly yet fairlyfrequently and some active foragers spendsuch a high percentage of the time in
continuous movement that their MPM valuesare necessarily low (Cooper et al., 2001). In thepresent study, the number and diversity ofspecies sampled did not represent the fullrange of foraging diversity for MPM withineither Iguania or Autarchoglossa. However,the lower MPM for iguanians (all but onespecies) and the higher values for the twoteiids were typical of North American speciesstudied previously (Cooper et al., 2001).
That foraging speeds were unrelated to body
size in the 19 species in the regression analyseswas not surprising. Although maximum sprintspeed increases with body size (Van Dammeand Vanhooydonck, 2001), lizards forage at
much lower than maximum speeds. Ambushforagers necessarily have much lower averagethan maximum speeds because they aremotionless much of the time. Even whenattacking prey and moving from one ambushpost to another, maximum speeds are notneeded and might interfere with ability tocapture slow-moving prey. For active foragersthat spend much of the time moving, highspeed would interfere with searching ability,especially by species that rely on tongue-flicking to locate chemical cues from hiddenprey or that visually hunt for prey in litter orother complex substrates. Foraging speed inactive foragers must be slow enough to avoidexhaustion. Thus, foraging speed may beaffected by foraging modes and stamina and
must be much lower than maximal burst speed.For lizards in the size range of this study
(maximum SVL 51143 mm), body length didnot affect foraging speed. However, the sizerange here includes only a small portion of thesize range for lizards worldwide, which exhibit50-fold variation in SVL between tiny geckosand the largest varanids. Foraging speedsmight be affected by body length if a broaderrange of body size is considered. Nevertheless,the lack of relationship between foraging speed
and body length in the size range used here isimportant because it applies to a large majorityof lizards in many regions. For example, in thegeographical area covered by Conant andCollins (1998), none of 72 species indigenousto the USA are smaller than species in theanalysis and only five anguids and a singlephrynosomatid (Sceloporus serrifer) are larger.Thus, 92% of species are in the size range ofspecies in this study. The larger anguids moveslowly, suggesting that body size may not have
a strong effect for them, either. Many of thelargest species are herbivorous (e.g., Cooperand Vitt, 2002; Pough, 1973), including igua-nas, and thus are excluded from studies of
TABLE 4.Correlations between phylogenetically inde-pendent contrasts for pairs of foraging variables for 19
species. * Significant at P , 0.001.
PTM MPM AS MS
PAM 0.84* 0.35 0.50 0.17PTM 0.34 0.34 0.20MPM 0.28 0.06AS 0.03
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search modes in carnivores. Thus, the findingssuggest that effects of body size on foragingspeed are likely to be negligible except when
very small geckos or very large active foragers
such as varanids, the largest teiids and skinksare compared with other lizards.Foraging speeds differed dramatically be-
tween lizard clades. The two teiids studied hadaverage speeds 15 times greater than theiguanians, but their speed while moving wasonly about one tenth that of the iguanians. Inthe comparison adding five species of Africanlacertids, the difference in average speedbetween iguanians and autarchoglossans wasslightly greater, but the difference in speed
while moving was reduced, autarchoglossanshaving a speed while moving slightly greaterthan one fourth that of iguanians. Differencesin foraging modes may account better fordifferences in foraging speed than phylogenyalone, but too few data are available to conducta meaningful test for an effect of foraging modeindependent of phylogeny. However, differ-ences between analyses by phylogenetic groupand foraging mode are attributable to inclusionof one ambush forager, Meroles knoxii (PTM 50.07), one of several ambushers in a family
composed primarily of active foragers (Arnold,1990; Perry et al., 1990).
PAM differed greatly between both taxo-nomic groups and foraging modes. Althoughthis variable was conceived as a possibly reli-able way to determine differences amongspecies in methods of searching for prey(Cooper and Whiting, 1999), present evidenceis inadequate to assess the effect of foragingmode independent of phylogeny on PAM.Nevertheless, the single species for which
a transition from ancestral active foraging toambush foraging has occurred, PAM hasdecreased. In another lacertid that has atypi-cally low PTM, yet is an active forager, PAM isalso atypically low. To assess the importance offoraging modes to PAM, data on PAM, foragingspeeds, and the other foraging variables areneeded for multiple taxa representing lineagesin which evolutionary shifts in foraging modehave occurred.
Relationships between Foraging Variables
Relationships involving PAM and foragingspeeds are of interest because they have notbeen reported previously for speed and data for
PAM have included only North Americanspecies (Cooper et al., 2001). As reportedpreviously for a smaller sample of species,PAM and PTM are very highly correlated when
species are considered independent. Althoughthe previous study (Cooper et al., 2001) foundno significant relationship between PAM andPTM in an analysis accounting for phylogeneticrelationships, these variables were stronglyrelated in this study using a larger andtaxonomically broader sample.
In part, a strong relationship between PAMand PTM is inevitable because a predator thatspends a greater percentage of its time movingis expected by chance to locate and attack preya greater proportion of the time while moving.For the limited data, it appears that activeforagers may discover and attack prey whilemoving at a higher percentage of the time thanthey spend moving and that ambush foragersmay attack prey while moving at a lowerpercentage of the time than they spendmoving. Foraging movements by ambushersare usually attacks on prey or shifts to newambush posts, whereas movements and searchare combined by active foragers.
In the independent species analysis, average
speed was negatively related to speed whilemoving and positively to PAM and PTM,
whereas speed while moving was negativelyrelated to both PAM and PTM and hada marginal negative relationship with MPM.These relationships conform to predictionsbased on differences in searching behavior,but were not significant in the analyses usingindependent contrasts. However, the correla-tion between average speed and PAM was sug-gestive. The relationships of foraging speeds to
other foraging variables merit further investi-gation in comparative studies with a largersample size and representing several majorshifts in foraging behavior within lineages.Foraging speed variables may be importantfor characterizing lizard foraging behavior andclarifying the existence of discrete foragingmodes.
MPM and PTM were not significantlycorrelated in either tips or independentcontrast analyses. This contrasts with a signifi-
cant tips correlation (r5
0.73) reported byCooper et al. (2001). Present results are morereliable because the sample is more than 50%larger and more taxonomically diverse than in
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previous work. PTM and MPM need not berelated because a species that moves a fixedpercentage of the time may divide movementsinto bouts of variable duration and number.
Independence of PTM and MPM suggests theimportance of considering both variablessimultaneously when characterizing lizard for-aging behavior (Butler, in press).
Acknowledgments.We are grateful to E. Martins forhelp with use of COMPARE. WEC is grateful to J. Dixonfor valuable advice about field sites in Texas and toT. Vanzant, S. Lerich, and M. Pittman for permission to doresearch and hospitality at the Black Gap and ElephantMountain Wildlife Management Areas in Texas. WECthanks D. Wilson of the American Museum of NaturalHistorys Southwest Field Station for hospitality duringfield work and R. Cox for suggesting field sites in theChiricahua Mountains. We thank R. Van Loben Sels forhospitality during filed work in the Chiricahuas. SFFthanks the Wichita Mountains National Wildlife refuge forpermission to conduct observations under permit 56841.
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Accepted: 7 March 2005Associate Editor: Michael Dorcas
Herpetologica, 61(3), 2005, 259267
2005 by The Herpetologists League, Inc.
THE ILIOSACRAL ARTICULATION IN PSEUDINAE(ANURA: HYLIDAE)
ADRIANA S. MANZANO1,3 AND MONICA BARG2
1CICyTTP-CONICET, Matteri y Espana, (3105), Diamante, Entre R os, Argentina2CONICET, Fac. de Biolog a, UNMDP
We analyzed the iliosacral joint and iliolumbaris muscle anatomy of the species of Pseudinae, based on thetwo types of articulations defined by Emerson. Unusual characters should be expected in the pseudineiliosacral articulation structure, given their aquatic habits and evolutionary history. In fact, the presence ofa ligamentous cap joining the ilium with the sacral diapophysis has not been described previously, and may beunique to pseudines. This particular group lacks a single pattern of iliosacral articulation for the wholesubfamily, and the articulations are not strictly referable to any of the types or subtypes described by Emerson.The iliosacral articulation is interspecifically variable within Pseudinae and is intermediate between thearticulations of Type IIA and IIB.
Key words: Anura; Hylidae; Iliosacral articulation; Ligamentous cap; Pseudinae
THE PELVIS of anurans generally is formed by
three pairs of elements (ilium, ischium and
pubis) that show some modifications within
modern anurans. Within Neobatrachia, thepelvis has been described as a stable structureformed by the ilium and the ischium, leavingthe pubis as a reduced, nonossified cartilage,3 CORRESPONDENCE: e-mail, [email protected]
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with different degrees of mineralization(Trueb, 1973) in various taxa. There are some
variations in the anuran pelvis that have beendescribed before; for example, the presence of
pre-pubic bones in Leiopelmatids, somePipids (Cannatella and Trueb, 1988; Trueb,1973), and Discoglossus sardus (Clarke, 1988;Pugener and Maglia, 1997), and post-pubicelements in Ascaphus truei. Additional ele-ments can be mineralized or remain cartilag-inous. These variations, and some related tothe shape of pelvic bones, have been used inphylogenetic analyses (e.g., by Heyer, 1975;Inger, 1972; Lynch, 1973).
The expansion of the sacral diapophyses andtheir ventral joint with the ilium is a character-istic that makes modern anurans uniqueamong the existing vertebrates (Jenkins andShubin, 1998; Trueb, 1973). The arrangementof the iliosacral joint elements were catego-rized by Emerson (1979), who demonstratedthat the type of articulation and its possiblemovements are related to the different formsof anuran locomotion. Emerson defined twotypes of articulations (I and II) based on theextension of the sacral diapophysis, the posi-tion and shape of the sesamoids, and the origin
and insertion of the articular ligaments inextant anurans. The iliosacral articulationforms a functional complex with the muscleIliolumbaris that is responsible for the move-ment of the pelvis during locomotion (Emer-son, 1979; Whiting, 1961).
Herein, we describe and analyze the ilio-sacral functional complex within some speciesof the two genera of the hylid subfamilyPseudinae (Duellman, 2001). Pseudinae is anessentially aquatic group of South American
anurans with characters that lead to contro-versial interpretations, such as the presence ofintercalary elements and an opposable thumbof the manus (Cei, 1980; Manzano, 1996).Functionally, opposable thumbs are associatedmore closely with an arboreal than an aquaticlifestyle, and are characters that are shared
with other anuran groups, such as somePhyllomedusinae, Rhacophoridae, and Man-tellidae.
Although Pseudinae seem to be a mono-
phyletic group, it is difficult to separatepseudids from the Hylidae and Centrolenidae(da Silva, 1998; Ford and Cannatella, 1993). DaSilva (1998) undertook a phylogenetic analysis
including Allophryne, Centrolenidae, Hylidae,and Pseudidae, and presented evidence thatPseudidae belongs within Hylidae, as a sistergroup of Hylinae. Subsequently, Duellman
(2001) included Pseudinae as a subfamily ofHylidae.We accept Duellmans (2001) classification
of Pseudinae. Nevertheless, there is still muchto understand about the morphology andevolutionary relationships of this group, whichincludes variations of morphological novelties,(e.g., those of the iliosacral joint).
In this study, we focus our interest on theanalysis of the iliosacral anatomy of the speciesof Pseudinae, based on the two types of articu-
lations defined by Emerson (1979, 1982). Giventheir aquatic habits and shared evolutionaryhistory, unusual characters could be expectedin the pseudine iliosacral articulation structure.
MATERIALS AND METHODS
We dissected and observed the iliosacralarticulation and associated musculature of 25specimens of Pseudinae, five specimens ofCentrolenidae, and six specimens of otherHylidae (see Appendix I). The specimens were
subjected to differential staining methods tostudy musculature based on a modification of
Wassersugs (1976) technique. The modifica-tion involves almost the same steps required forstaining bones and cartilages, with differencesin the time that the specimens remain in thesolutions, depending on their size. Specimenspreviously skinned and preserved in 10% form-aldehyde, were washed in tap water for a periodof two hours before introducing them ina solution of Alcian Blue in Absolute Alcohol
and Acetic Acid. After 12 days in the dyesolution, the cartilage in a medium size frog,would take on a blue color; the specimens werethen fixed in Absolute Alcohol (3 h). In the nextstep, thematerial was introduced intoa solutionof Potassium Hydroxide for approximately 2minutes to neutralize the acid of the AlcianBlue solution. After that, specimens were keptfor 12 days in a solution of Red alizarin inPotassium Hydroxide. Once the specimenbones were dyed red, the specimen was
preserved in 70% ethanol, avoiding musclemaceration. With this technique, bones stainred, cartilage stains blue, and muscles remainunstained and can be observed intact.
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To study the articulation in detail, weembedded two specimens in paraffin for his-tological sections (Anderson and Bancroft,2002), one of Pseudis minuta (FML03676)and one ofLysapsus limellus (DIAM 019), andstained them with hematoxilin-eosin accordingto the standard staining procedure for paraffinsections (Wilson and Gamble, 2002). Thespecimens were examined with the aid of aOlympus stereo microscope equipped with
a camera lucida and photographs were takenwith a camera attached to the microscope.Pseudis minuta was used as a reference
species, with descriptions of the articulationand morphology of its iliolumbaris muscle. Theremaining species of Pseudinae and its sub-species were compared to P. minuta. Wefollow the terminology of Trueb (1973) forosteology and Gaupp (1896) for musculature.
Two specimens ofPseudis minuta were video-recorded with a GR-VL505 JVC camera to allow
analysis of the movements of the pelvic girdleduring swimming and resting. A specimen ofXenopus laevis also was video-recorded forcomparison.
RESULTS
The Iliosacral Articulation
Pseudis minuta (Fig. 1).The sacral dia-pophyses are narrow, dorsoventrally com-pressed (with an elliptic transversal section)and oriented posterolaterally. The distal mar-gin of the sacral diapophysis is almost com-pletely mineralized and not expanded. An oval,
well-developed sesamoid is present on the
lateral edge of the sacral diapophysis. Theshaft of each ilium extends anteriorly wellbeyond the sacral diapophysis, reaching themid-level of the Presacral Vertebra VIII. Anexpanded ligament arises from the anteriorend on both margins of the iliac crest, andcovers dorsally the anterior end of the iliacshaft. Laterally, the ligament encloses theterminus of each sacral diapophysis, forminga ligamentous cap and incorporating thesesamoid to this structure. This ligamentous
cap inserts on the dorsal surface of the sacraldiapophysis, including the anterior and poste-rior edges of the lateral terminus of this bonystructure. The M. iliolumbaris originates as
FIG. 1.Pseudis minuta (FML:03676-1). (A) Photograph of dorsal view of the iliosacral articulation; (B) drawing ofFigure 1A, dorsal view of the iliosacral articulation. dc, dorsal crest; il, iliac shaft; lc, ligamentous cap; sd, sacraldiapophysis; ses, sesamoid; u, urostyle. Scales 5 1 mm.
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a tendon on the ligamentous cap, from the
anterior region of the iliac crest. Lateralprocesses of presacral Vertebrae VII and VIIIare oriented anterolaterally and as long as thesacral diapophysis. The lateral processes of theresting presacral vertebrae are oriented pos-terolaterally.
Other species of Pseudis.The subspeciesofP. paradoxa (P. p. paradoxa, P. p. occidenta-lis and P. p. platensis) that we describe show anarrangement of the elements that conforms tothe articulation described for P. minuta (Fig.
1). Nevertheless, the form and size of thesesamoid within P. paradoxa is more roundedthan oval and relatively larger, being almost aslong as the width of the lateral end of the sacraldiapophysis (Fig. 2). In this species ofPseudis,the distal tips of each sacral diapophysis isat least partially mineralized. Within the sub-species of P. paradoxa, the articular ligamentoriginally described by Emerson (1979, 1982)is not evident, but a ligamentus cap is present.The articular ligament of P. cardosoi and P.
bolbodactyla, like that of P. minuta, has aninsertion on the mid-dorsal region of eachsacral diapophysis and is included in the liga-mentous cap. Except for P. bolbodactyla, the
length of the iliac shafts of Pseudis species is
very homogeneous, extending anteriorly to thesacral diapophysis and reaching the mid-levelof presacral vertebra VIII. In P. bolbodactyla,the iliac shafts extend to the anterolateralborder of the sacral diapophysis. There is aniliac crest present in all species studied, but
with variation in size and length.In the histological sections of the iliosacral
joint, we observed a combination betweenType IIA and IIB articulation for the species ofPseudis (Fig. 3). The tip of the sacral diapoph-
ysis is curved ventrally, with a wedge-likesesamoid, located laterally (as in a Type IIAarticulation). Although, in the histologicaltransversal section, the form of the ilium andthe diapophysis with its small cartilaginoustip, correspond to Type IIB articulation. Theligamentous cap envelopes the ilium ventro-laterally and the sesamoid laterally, and insertson the mid-dorsal surface of the sacraldiapophysis.
Lysapsus limellus.The condition of
Lysapsus limellus is intermediate betweenTypes IIA and IIB (Emerson 1979, 1982).The sacral diapophyses are expanded laterally
with a cartilaginous distal border that is larger
FIG. 2.Pseudis paradoxa platensis (FML: 004661-1). (A) Photograph of dorsal view of the iliosacral articulation;(B) drawing of Fig. 2A, dorsal view of the iliosacral articulation. cd and dc, dorsal crest; il, iliac shaft; lc, ligamentous cap;sd, sacral diapophysis; ses, sesamoid; u, urostyle. Scales 5 1 mm.
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than that of Pseudis (see Figs. 3, 5). Theligamentous cap envelopes the lateral border
of each sacral diapophysis, the anterior ex-treme of the iliac shaft, incorporating thesesamoid, and a very differentiated internalarticular ligament. The articular ligamentinserts on the mid-dorsal region of the sacraldiapophysis and the insertion is not close to the
vertebral body as in Emersons Type IIAiliosacral articulation. The lateral processes of
Presacral Vertebrae VIII is as long as the sacraldiapophysis (as in Emersons Type IIB articu-
lation) and is oriented strongly anterolaterally.The oval sesamoids are smaller than those ofPseudis, and cover only a third of the antero-lateral edge of the sacral diapophysis (Fig. 4).The iliac shaft extends anteriorly as far as theposterior border of the Presacral Vertebra VIIand has a small, short longitudinal crest.Histological sections of the pelvic girdle inLysapsus, show a Type IIA iliosacral articula-tion (Fig. 5), and like Pseudis minuta, the tip ofthe sacral diapophysis is curved ventrally and
the sesamoid is positioned laterally. The formand position of each sesamoid with respect tothe ilium and the insertion of the ligament alsois similar to the condition seen in Pseudis
minuta (Figs. 3, 5). Ilium tips are completelyenveloped by the ligamentous cap.
The Muscle Iliolumbaris
Pseudis minuta.In Pseudis minuta (Fig. 6),the Iliolumbaris muscle has a wide origin bya tendon on the ligamentous cap, positioned on
the anterolateral region of the shaft of the iliumand the anterolateral portion of the sacraldiapophysis. This muscle inserts on the lateralprocesses of Presacral Vertebrae VVIII, and
FIG. 3.Lysapsus limellus (FML: 00725-1). (A) Photograph of dorsal view of the iliosacral articulation; (B) drawing ofFig. 3A, dorsal view of the iliosacral articulation. dc, dorsal crest; il, iliac shaft; illm, M. Iliolumbaris; la, articular ligament;lc, ligamentous cap; sd, sacral diapophysis; ses, sesamoid; u, urostyle. Scales 5 1 mm.
FIG. 4.Pseudis minuta (FML03676-2). Histological
section of the right iliosacral articulation, transversal view.il, ilium; lc, ligamentous cap; sd, sacral diapophysis; ses,sesamoid; arrows show the insertion point of theligamentous cap. Scale 5 0.5 mm.
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lies parallel to the Longissimus Dorsi muscle,covering most of the external surface of thelateral processes of Presacral Vertebrae VI
VIII. It is a thick, wide muscle with transversetendinous inscriptions by which it inserts to thetip of each of the lateral processes of Presacral
Vertebrae VVIII. An incipient division of themuscle into two branches at the origin wasobserved, with the lateral branch being moredeveloped and thicker than the medial one.
Other Pseudines.In Pseudis paradoxaplatensis and P. p. occidentalis, the Iliolumba-ris muscle originates on the ligamentous capby a short tendon, as was observed in P.
minuta. It is present as single muscle and,although two bundles of muscle fibers aredistinguishable, no division is observed. This
muscle inserts on the lateral process of thePresacral Vertebrae IVVIII.
Lysapsus limellus.In Lysapsus limellus,the Iliolumbaris muscle is undivided and hasa narrow origin on the anterolateral portion ofthe iliac shaft. It inserts on the tips of eachlateral process of Presacral Vertebrae IVVIII.
Monitoring Locomotion in Pseudis minuta
In the video-recording, we observed that
Pseudis minuta swims by moving the posteriorlimbs without evident rotation of the iliosacralarticulation. Thelegmotion is practicallylimitedto flexions and extensions of the tibiofibula and
foot (i.e., tarsometatarsus). When the animalsfoot is in contact with the substrate (a sub-merged rock or the aquarium floor), the swim-ming movement is propelled by a kick.
Most of the time specimens of this speciesremain floating with their heads out of the
water and their webbed feet expanded atthe same level as the head, partially out of the
water. The back is curved dorsally in a concavearc and the iliosacral articulation appears toform an angle smaller than 1708, compared
with the iliosacral articulation of Rana cat-
esbiana in a resting position (shown in Jenkinsand Shubin, 1998: Figs. 9A, 10A).
DISCUSSION
The morphology of the iliosacral articulationin pseudines does not coincide completely
with any of the types described by Emerson(1979, 1982). Although some characteristics
would indicate a Type IIB iliosacral articula-tion in some pseudines, important variations
make it inappropriate to place them in thiscategory. Also, in some species, there isa combination of characteristics from bothtypes of articulation (IIA and IIB).
FIG. 5.Lysapsus limellus (DIAM 019-2). Histologicalsection of the left iliosacral articulation, transversal view.il, ilium; lc, ligamentous cap; sd, sacral diapophysis;ses, sesamoid; arrows show the insertion point of theligamentous cap. Scale 5 0.5 mm.
FIG. 6.Pseudis minuta. Dorsal view of the iliosacralarticulation. m.il.ext., M. Iliacus Externus; m. iliolum.l., M.Iliolumbaris Lateralis; m. iliolum.m., M. IliolumbarisMedialis; lc, ligamentous cap; ses, sesamoid; ssc, supra-scapulae. Scale 5 2 mm.
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The ligamentous cap described herein hasnot been described previously, and may beunique to pseudines. In the case of Pseudis,the non expanded, cylindrical shape of the sa-
cral diapophysis, the lateral processes of thepresacral vertebrae that are as long as thesacral diapophysis, and the presence of an iliaccrest would indicate a Type IIB iliosacralarticulation (Emerson, 1979). However, theinsertion of the ligamentous cap displacedfrom the lateral edges of the sacral diapoph-
ysis, as well as the absence of a well-definedligament (Emerson, 1982), suggest variationsin this pre-established pattern. Only in Lysap-
sus limellus was a well-defined ligament clearlydifferentiated from the ligamentous cap thatgenerally is observed; the articular ligament
was difficult to identify in Pseudis species,where it is included as a part of theligamentous cap. In Pseudis paradoxa thereis no evidence of the presence of the articularligament.
The insertion of the M. Iliolumbaris on thelateral processes of Presecral Vertebrae IV
VIII only, instead of all the pre-sacral verte-brae, and their wide origins on the ligamentouscap (except in Lysapsus), at the same level as
the lateral extremes of the sacral diapophysis,are other observed variations. These differ-ences are more evident in Lysapsus limellus,
where the sacral diapophysis are expanded, thesesamoid is small, and the insertion of theligamentous cap is closer to the mid-region ofthe sacral vertebra than in Pseudis. This wouldsuggest a Type IIA articulation, but thepresence of the iliac crest and the long lateralpresacral processes (such as in Pseudis) arecharacteristic of Type IIB articulation.
Nevertheless, except for the presence ofa defined ligament in Pseudis cardosoi, littlevariation in the morphology of the iliosacralarticulation in Pseudis was observed, especiallyamong the subspecies ofPseudis paradoxa.
Bigalke (1927) mentioned a proximal bi-furcation of the M. Iliolumbaris in Rana (R.esculenta, R. fusca, and R. arvalis) anddescribes an almost complete separation intwo branches in Bufo bufo (as Bufo vulgaris)
with or without tendinous origins. In pseu-
dines, the branches of the M. Iliolumbarishave various degrees of differentiation; themedial branch is present only in species ofPseudis, and although in P. paradoxa the
medial branch is not separated from the lateralbranch, it is identified easily. In Lysapsuslimellus the muscle shows no branch separa-tion. In all pseudines observed, the origin of
the muscle is on the ligamentous cap.In the remaining hylids analyzed, the di-vision of the muscle varies from an incipientbifurcation (Scinax acuminata) to a doublemuscle (Hyla pulchella and H. andina). InCentrolenidae the muscle is single and origi-nates from the iliac shaft. All centrolenidsexhibit a Type IIA articulation, but also withsome variations. The sacral diapophysis areexpanded, there is no crest in the iliac shaft,they have long ovate-shaped sesamoids (widestat the base), and the articulary ligament insertson the distal edge of each sacral diapophysis(as in Type IIB). The ilium reaches the dia-pophysis anteriorly, not overlapping it.
Emerson (1979) considers that the patternof iliosacral articulation is family specific,except in Hylidae, Microhylidae, and Disco-glossidae. Additionally, she recognize theexistence of exceptions within Atelopus, Den-drobates, and Leptopelis, and associated themto the differences in locomotion of thosespecies (Emerson, 1982, 1988). Similarly, the
subfamily Pseudinae, recently classified withinHylidae (Duellman, 2001), not only lacksa single pattern for the whole subfamily, butalso the articulations are not strictly referableto any of those types and subtypes describedby Emerson. The iliosacral articulation inPseudinae is intermediate between the articu-lation Types IIA and IIB, and shows interspe-cific variations.
The ability to jump is present in some formin all anurans (Duellman and Trueb, 1986),
but is limited by the flexibility of the trunk andiliosacral articulation (Jenkins and Shubin,1998; Trueb, 1996). The anurans that are good
jumpers have a very flexible iliosacral articu-lation (Green, 1931) with anteroposterior androtational movements that, together with thesacral-urostilic articulation, align the vertebralcolumn with the pelvic girdle during jumping(Jenkins and Shubin, 1998; Kargo et al., 2002).Some authors consider that aquatic anuranshave a movement and design similar to those
of saltatorial specialist jumpers, propellingthemselves with a kick (Emerson, 1982; Gansand Parsons, 1965); although, others (Abour-achid and Green, 1999) state that these could
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be independently derived locomotory trends.Kargo et al. (2002) demonstrated that theiliosacral articulation is a gliding joint, in whichthe trunk translation and rotation are in-
dependent of one another. Emerson and deJongh (1980) hypothesized that this transla-tion of the trunk could be important duringswimming, and is observed in frogs that arespecialized for swimming.
In pseudines, the movement during swim-ming is propelled mainly by the flexion of thetibiofibula and the foot (tarsometatarsus), andflexion of the knee seems to be minimal ornonexistent. Except when the animal rests onthe waters surface, it swims by a jumping-stylemovement of the legs. This kind of movement,
which mainly involves the distal elements ofthe legs (tibiafibula and tarsometatarsus), wasdescribed previously for Hymenochirus boett-
geri (Gal and Blake, 1988), but for theadjustment of direction rather than propul-sion. In a common jumping frog like Rana
pipiens, the involvement of the distal elementsof the hind limbs could increase the jumpdistance (Kargo et al., 2002). Interestingly,Pseudis also is a very good jumper during anexplosive escape response (A.S. Manzano and
M. Barg, personal observation).The iliosacral articulation acts as the main
mechanical axis during jumping, transmittingthe impulse from the legs towards the
vertebral column. In this movement, thevertebral column aligns with the pelvic girdleand the angle of the iliosacral articulationrotates, from 1208 (in resting position), to 1708(in jumping positions) (Callow and Alexander,1973). During swimming, the iliosacral artic-ulation seems to be less important comparing
with the movements of the legs.In specimens ofPseudis that are resting andfloating, the angle formed by the iliosacral jointseems to increase from the 1708 angle duringswimming as a consequence of the dorsallycurved, concave position of the back. In otherresting, aquatic anurans, the vertebral columnremains aligned with the pelvic girdle (e.g.,
Xenopus laevis, A.S. Manzano and M. Barg,personal observation). It is known that in
Xenopus laevis the iliosacral joint is fused and
akinetic (Jenkins and Shubin, 1998).Although, a broad, cuff-like ligament joiningthe ilium with the sacral diapophisis has beendescribed in pipids (Trueb, 1996), the mor-
phology of iliosacral articulation in pseudinesis quiet different. In pipids cuff-like ligamentcovers all the sacral vertebrae between the ilia.Among pipids, the greatly expanded sacral
diapophyses and cuff-like ligaments restrictthe movements of the iliosacral articulation toan anterior to posterior sliding movement.
A combination of characters of Type IIAand IIB iliosacral articulation in Lysapsuslimellus, like the expanded sacral diapophysesand long lateral processes of the Presacral Ver-tebras could reduce considerably the lateralrotating movements of the iliosacral articula-tion, but in this case (Lysapsus limellus), thelateral processes of the Presacral Vertebrasare strongly anterolaterally oriented thus thelateral rotating movement are not limited.
The presence of the ligamentous cap in theiliosacral articulation of the species ofPseudiscould increase the range and angle articulationduring the transition from resting to swim-ming positions, acting as a hinge and addingfreedom to the movement of rotation. The
variations in the morphology of the iliosacralarticulation may or may not imply mechanical
variations in its movement, but can contributeto the hyperextension of the back during rest.
Acknowledgments.We are very grateful to T. Burton,J. Faivovich, G. Perotti and I. Vaquilla for critically readingour manuscript. We thank V. Casco and F. Izaguirrefor thehistological sections and E. Lavilla for helping us with thephotographs. We also thank the referees of Herpetologicafor the valuable suggestions to improve the manuscript.Supported by PICT 12418 and PEI 6155.
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Accepted: 27 March 2005Associate Editor: Christopher Sheil
APPENDIX I
Specimens Examined
Specimens belong to the Herpetological Collections of
Museu de Historia Natural, Campinas, Sao Paulo, UNI-CAMP (ZUEC); Museu de Ciencias e Tecnologia daPUCRS, Brazil (MCP); Carnegie Museum (Carn. Museum);Museo Argentino de Ciencias Naturales (MACN); Funda-cion Miguel Lillo (FML); Universidad de Corrientes(UNNEC); CICyTTP-CONICET Diamante, Entre Ros,Argentina (DIAM); Fundacion La Salle de CienciasNaturales, Venezuela (EF).
Family Hylidae: Subfamily PseudinaePseudisbolbodactylus ZUEC 11800, ZUEC 11801; P. caribensisEF-112, 13554; P. cardosoi MCP 3375, MCP 3775; P.paradoxa paradoxa Carn. Museum 49512; P. paradoxaoccidentalis MACN 37698, MACN 37699, FML00708(2 specimens); P. minuta MACN 37700, MACN 37701,
MACN 37702, FML03676 (1 specimen for histologicalsections, 1 for photograph); P. paradoxa platensis UNNEC03455, FML00936 (2 specimens); P. paradoxa FML04661(2 specimens, photographs); Lysapsus limellus FML 00791(photograph), FML 00725, DIAM 019 (2 specimens, onefor histological sections). Two living specimens of Pseudisminuta, male and female, were video-recorded andphotographed; they remain in an aquarium in M. Bargpossession at the University of Mar del Plata, Argentina.Subfamily PhyllomedusinaePhyllomedusa hypochon-drialis FML 04286. Subfamily HylinaeScinax nasicumDIAM 023; S. squalirostris DIAM021; Phrynohyasvenulosa DIAM 024; Hyla andina DIAM 022; H. pulchellaDIAM 038.
Family CentrolenidaeHyalinobatrachium aureogu-tattum DIAM 055; Centrolene robledoi DIAM 056;C. geckoideum DIAM 075; C. grandisone DIAM 076;Cochranella ignota DIAM 057.
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