BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofitpublishers, academic institutions, research libraries, and research funders in the common goal of maximizing access tocritical research.

Jumping Behavior of Semiterrestrial Tadpoles of Indiranabeddomii (Günth.): Relative Importance of Tail and Body SizeAuthor(s): Dheeraj K. Veeranagoudar, Rajkumar S. Radder, Bhagyashri A.Shanbhag, and Srinivas K. SaidapurSource: Journal of Herpetology, 43(4):680-684. 2009.Published By: The Society for the Study of Amphibians and ReptilesDOI: http://dx.doi.org/10.1670/08-158.1URL: http://www.bioone.org/doi/full/10.1670/08-158.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in thebiological, ecological, and environmental sciences. BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies, associations,museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated contentindicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercialuse. Commercial inquiries or rights and permissions requests should be directed to theindividual publisher as copyright holder.

SHORTER COMMUNICATIONS

Journal of Herpetology, Vol. 43, No. 4, pp. 680–684, 2009Copyright 2009 Society for the Study of Amphibians and Reptiles

Jumping Behavior of Semiterrestrial Tadpoles of Indirana beddomii (Gunth.): RelativeImportance of Tail and Body Size

DHEERAJ K. VEERANAGOUDAR, RAJKUMAR S. RADDER,1 BHAGYASHRI A. SHANBHAG, AND

SRINIVAS K. SAIDAPUR2

Department of Zoology, Karnatak University, Dharwad-580 003 India

ABSTRACT.—This study examined the jumping pattern and its relationship with various body traits insemiterrestrial tadpoles, Indirana beddomii. The tadpoles were separated into four groups based on theabsence (Group I) or presence (Group II) of functional hind limbs, presence of forelimbs (Group III), and atmetamorphic climax (Group IV). During early developmental stages, tadpoles are able to move by flippingand jumping not only forward but also sideways and backward. Prior to takeoff, they usually wag the tail,possibly providing thrust to takeoff. However, in later developmental stages, hind limbs are used for takeoff. In Group I tadpoles, the tail was three times longer than SVL and contributed to jumping performance.In Groups II and III, both SVL and hind-limb length were positively correlated to jumping performance. Inthe Group III, forelimb length was also correlated with jumping performance. However, stepwise multipleregression analysis showed that, in Group II, hind limbs and, in Group III, forelimbs contributed to jumpingperformance. Thus I. beddomii tadpoles use their tails for jumping at early stages and limbs at later stages.Upon reaching metamorphic climax and thereafter, the correlations between jumping performance and SVLand hind- or forelimb length was lost. Lack of correlation between the body traits and jumping performanceduring metamorphic climax may be attributed to physiological and anatomical changes occurring during thisphase.

The life history of anurans is generally character-ized by early larval stages adapted to an aquaticenvironment and adult stages adapted to diverseterrestrial habitats. Swimming during aquatic larvalstages and jumping following metamorphosis aretypical modes of locomotion in anurans. There areseveral studies on the swimming dynamics ofamphibian tadpoles (Watkins, 1997; Hoff and Was-sersug, 2000; Wilson et al., 2000) and on the jumpingperformance of metamorphosed frogs (John-Alderand Morin, 1990; Semlitsch et al., 1999; Tejedo et al.,2000a,b). Although the majority of anurans have fullyaquatic tadpoles, a few species have semiterrestrialtadpoles. For instance, tadpoles of Petropedetes parkeri,Cycloramphus sp., Thoropa sp., and Indirana beddomiiare semiterrestrial (Hoff et al., 1999). These tadpolesdiffer in their morphology from purely aquatic forms,especially in their long tails with reduced fins(Haddad and Prado, 2005) that suit their specializedlocomotion at water-land interface.

During field studies in the Western Ghats, weencountered tadpoles of I. beddomii. They were foundjumping on the moist latterite rocks, in and out ofsmall approximately 1-cm deep holes in the rock inresponse to intermittent showers (June throughAugust) typical in that area. The first brief descriptionof I. beddomii tadpoles was given by Annandale (1918),and recently by Kuramoto and Joshy (2002), and notedskipping or hopping by these tadpoles. To the best ofour knowledge, no systematic studies on jumping insemiterrestrial tadpoles have been carried out. Hence,the present study was designed to understand moreabout jumping in these tadpoles at different stages ofdevelopment and metamorphic climax and the influ-

ence of SVL, tail, and forelimb and hind-limb lengthson jumping performance in semiterrestrial I. beddomiitadpoles.

1 Deceased 31 May 2008.2 Corresponding Author. E-mail: saidapur@gmail.

com

FIG. 1. Tadpoles of Indirana beddomii during differ-ent stages of development: (A) tadpole prior tofunctional hind limbs (Group I); (B) tadpole withwell-developed hind limbs (Group II); (C) tadpolewith both fore- and hind limbs (Group III).

MATERIALS AND METHODS

The study site, Sural village, Goa state (15u409N,74u109E), is situated at the top of a high mountainrange (1,828.8 m a.s.l) in southern Western Ghats ofIndia where I. beddomii tadpoles are encountered fromJune through August. They are found on the surfacesof laterite rocks that are covered with numerousdepressions or holes (approximately 1 cm diameter/depth). We collected tadpoles (N 5 77) of differentdevelopmental stages and categorized them into fourgroups: Group I: tadpoles prior to development offunctional hind limbs (Fig. 1A, N 5 20); Group II:tadpoles with functional hind limbs but prior toforelimb emergence (Fig. 1B, N 5 20); Group III:tadpoles with both hind and forelimbs (Fig. 1C, N 5

20); Group IV: tadpoles in metamorphic climax withor without rudimentary tail and metamorphs (N 5

17).Jumping trials were conducted in the field on three

consecutive days between 0800 and 1600 h (ambienttemperature 23.5 6 1uC). Tadpoles were induced tojump on a flat platform (approximately 0.6 3 2.6 m)located on the study site. Moist continuous-feedprinter paper was spread over the platform beforethe trials. Tadpoles were quickly placed in a Petri dishcontaining a thin layer of fountain pen ink to color its

ventral side. It was then placed at one end (startingpoint) of the paper and gently touched by a thin grassblade thereby inducing it to jump until it got fatigued.Jumping trials were recorded with a hand held videocamera by standing near the platform on whichtadpoles were allowed to jump. Generally, focalspecimens made more than 10 jumps in a given trial(average 16 6 3 jumps). Only specimens that mademore than 10 consecutive jumps in a linear trajectorywere included in data analysis. Individuals thatreversed their jump directions were excluded. Theblots left on paper were used to measure jumpdistances (hereafter, referred to as jumping perfor-mance) following the procedure of Tejedo et al.(2000a). Linear distance between two successive blotswas measured using the center point of each mark.Jumping performance of a given individual wasdetermined by considering the mean of the 10 longestjumps (cm). After the trials, snout–vent length (SVL),tail, forelimb, and hind-limb lengths were measuredto the nearest millimeter. Specimens were thenreleased. Voucher specimens are deposited in theDepartment of Zoology, Karnatak University, Dhar-wad.

Because each group consisted of individuals ofvarious sizes, variation in jumping performance

FIG. 2. Jumping patterns of Indirana beddomii tadpoles. Arrow indicates direction of movement. (A) Flippingmovement of early stage tadpole induced to jump. The figure shows a series of flipping actions in the air fromthe starting point at the extreme right. (B) Takeoff and landing postures of a tadpole with functional hind limbs.(C) Jumping pattern of a newly metamorphosed froglet that takes off with hind limbs and lands using forelimbs.

SHORTER COMMUNICATIONS 681

among members of a given group was determined bycomputing the coefficient of variation (CV) to reflectthe extent of variation in jumping performance amongindividuals within a group. Variations, if any, in SVL,tail, fore- and hind-limb lengths among individuals ofdifferent groups were analyzed using one-way AN-OVA followed by Scheffe’s multiple range test.Variation with respect to forelimb length betweenGroups III and IV was determined by independentsample t-test. The relationship between jumpingperformance and body parameters was determinedby Pearson’s correlation coefficient analyses. Stepwisemultiple regression analysis was carried out todetermine relative contribution of each trait tojumping performance.

RESULTS

Indirana beddomii tadpoles exhibit different patternsof locomotion prior to formation of functional hindlimbs. These include crawling on the rock surface,climbing the moist smooth rock surface, flippingsideways or backward, skipping, and jumping. Theyjump not only in the forward direction but alsosideways or backward. When crawling, the tadpoleswaggle their body and tail slowly and move in aforward direction. Prior to takeoff, they usually startwagging their tail. Initially, tail wagging is slow, butsoon it becomes rapid. The tadpole then takes off byjumping or flipping in the desired direction (Fig. 2A).

Crawling and flipping movements become rare inlater stages of development. Later, when functionalhind limbs develop, tadpoles use them to take offfrom the ground and also for landing. They seem touse their tail for balancing and spring action (Fig. 2B).In later stages, jumping is generally in the forwarddirection (Fig. 2C).

Body Traits and Jumping Performance during Develop-mental Stages.—Mean SVL, tail length, fore- and hind-limb lengths, and jumping performance by tadpoles ineach of the four groups is given in Table 1. TadpoleSVL increased with developmental stage but not taillength.

In Group I tadpoles, tail length (but not SVL) waspositively correlated with jumping performance (Ta-ble 2) and also contributed to jumping performance(Table 3). Jumping performance varied moderatelyamong the members of this group (CV 5 21.1). InGroup II tadpoles, although jumping performancewas correlated with both SVL and hind-limb length(Table 2), only hind-limb length contributed to jump-ing performance (Table 3). Further, jumping perfor-mance was significantly greater than in Group Itadpoles. Jumping performance among individualsof this group varied moderately (CV 5 23.00). Meanjumping performance recorded in group III tadpoleswas greater than in Groups I and II tadpoles (Table 1)with moderate variation among group members (CV5 18.9). Jumping performance was positively corre-

TABLE 2. Shows correlation coefficient (r-values) of linear correlation analysis between jump performance(dependent variable) and morphological traits (independent variable) in Indirana beddomii.

Tadpoles prior tofunctional hindlimbs: (Group I)

(N 5 20)

Tadpoles withfunctional hind limbs:

(Group II)(N 5 20)

Tadpoles withfore- and hind limbs:

(Group III)(N 5 20)

Tadpoles at metamorphicclimax or newly

metamorphosed froglets:(Group IV) (N 5 17)

SVL (mm) 0.13 0.48* 0.62** 20.20Tail length (mm) 0.65** 0.16 20.48* —Forelimb (mm) — — 0.68** 0.30Hind limb (mm) 20.35 0.62** 0.63** 0.34

* Significant at 0.05 level; ** Significant at 0.01 level.

TABLE 1. Summary (mean 6 SD) of recorded traits of tadpoles and metamorphs in Indirana beddomii.Dissimilar letters indicate significant difference between groups based on one-way ANOVA followed byScheffe’s multiple range test.

Tadpoles prior tofunctional hindlimbs: (Group I)

(N 5 20)

Tadpoles withfunctional hind

limbs: (Group II)(N 5 20)

Tadpoles withfore- and

hind limbs:(Group III)(N 5 20)

Tadpoles atmetamorphic climaxor newly metamor-

phosed froglets:(Group IV) (N 5 17)

F/t- andP-values

SVL (mm) 5.10 6 0.72 a 10.33 6 1.05 b 11.48 6 0.57 c 11.56 6 0.70 c F3,76 5 297.05; P 5 0.00Tail length

(mm) 14.58 6 2.00 14.70 6 2.68 16.25 6 2.12 — F2,59 5 3.32; P 5 0.04Forelimb

(mm) — — 4.63 6 0.72 6.32 6 0.50 * t 5 28.17; P 5 0.00Hind limb

(mm) 1.90 6 0.65 a 14.48 6 2.16 b 18.38 6 1.27 c 19.21 6 1.54 c F3,76 5 551.63; P 5 0.00Jump

distance(cm) 8.28 6 1.75 a 13.56 6 3.20 b 20.40 6 3.93 c 22.64 6 3.55 c F3,76 5 79.64; P 5 0.00

* Significant difference between groups based on independent sample t- test.

682 SHORTER COMMUNICATIONS

lated with SVL and fore-, and hind-limb lengths andnegatively correlated with tail length (Table 2), butonly forelimb length contributed to jumping perfor-mance (Table 3). Mean jumping performance exhibit-ed by the tadpoles of Group IV was the greatestcompared to all other groups (Table 1), with the leastvariation within the group (CV 5 15.7). However,jumping performance was not correlated with SVL,hind- or forelimb lengths (Table 2).

DISCUSSION

Because semiterrestrial tadpoles spend a consider-able amount of time out of water and also move shortdistances in terrestrial habitat, it is expected that theywould differ in their morphology from fully aquatictadpoles. Although detailed comparison between thetwo types of tadpoles is not available, the develop-ment of forelimbs in fully aquatic tadpoles lags behindthat of the hind limbs by one stage, but in semiterres-trial tadpoles, the lag is usually about five stages (inAltig and McDiarmid, 1999). Annandale (1918) notedthe peculiarity of the long tail of I. beddomii tadpoles.Indeed, our study showed that the tail is three timesthe SVL in early stages (Group I) as has been found inOsteopilus brunneus, one of the most elongate tadpoleknown (Lannoo et al., 1987). In I. beddomii, there islittle or no increase in tail length until metamorphicclimax. After development of hind limbs in Group IItadpoles, a shift from tail-based locomotion (as inGroup I) to hind-limb dependent locomotion mayexplain the cessation of tail growth in tadpoles fromGroup II onward. At metamorphic climax, tail startsregressing, similar to that observed in other anurantadpoles.

A most remarkable feature of I. beddomii tadpoles intheir early stages (prior to the development offunctional hind limbs) is that they can jump in variousdirections (forward, backward, and sideways) upondisturbance. In these tadpoles, jumping performanceincreases with tail length but not with SVL. Althougha positive correlation between jumping performanceand hind-limb length and SVL is observed in Group IItadpoles, the hind-limb length is more important. Inthis developmental stage, tail wagging, and backwardand sideways jumps become rare, possibly because ofthe development of hind limbs. Thus, the tail mayplay a key role in jumping performance of early stagetadpoles, and in later stages it may merely help insteering or balancing during jumping. With theemergence of forelimbs in Group III tadpoles, fore-limbs mainly contribute to jumping performance.Forelimbs may help in adopting a proper ‘‘angle’’ ofjump that enhances jumping performance. By the timethe tadpoles reach metamorphic climax (Group IV)and thereafter, there is a loss of correlation betweenjumping performance and the body measurements.Possibly, physiological and anatomical changes oc-curring during the metamorphic climax place con-straints on locomotor consistency resulting in a lack ofcorrelation between the body traits and jumpingperformance.

It is of great interest to know the ecologicalcircumstances under which the tadpoles of I. beddomiihave taken to semiterrestrial habitat. These frogsbreed at higher elevations on the mountains ofWestern Ghats that receive torrential rains with

TA

BL

E3.

Sh

ow

sre

gre

ssio

nco

effi

cien

t(b

)an

dp

arti

alco

rrel

atio

n(r

)v

alu

eso

fst

epw

ise

mu

ltip

lere

gre

ssio

nan

aly

sis

for

Gro

up

sI,

II,

and

III

tad

po

les

of

Ind

iran

abe

ddo

mii

(ju

mp

per

form

ance

asd

epen

den

tv

aria

ble

and

bo

dy

trai

tsas

ind

epen

den

tv

aria

ble

s).

P,

0.05

issi

gn

ific

ant.

Tad

po

les

pri

or

tofu

nct

ion

alh

ind

lim

bs:

(Gro

up

I)(N

520

)T

adp

ole

sw

ith

fun

ctio

nal

hin

dli

mb

s:(G

rou

pII

)(N

520

)T

adp

ole

sw

ith

fore

-an

dh

ind

lim

bs:

(Gro

up

III)

(N5

20)

SV

L(m

m)

b5

20.

14;

r5

20.

17P

50.

49b

52

0.24

;r

52

0.15

P5

0.53

b5

0.25

;r

50.

22P

50.

37T

ail

len

gth

(mm

)b

50.

65;

r5

0.65

P5

0.00

b5

0.12

;r

50.

15P

50.

52b

52

0.31

;r

52

0.41

P5

0.08

Fo

reli

mb

(mm

)—

—b

50.

68;

r5

0.68

P5

0.00

Hin

dli

mb

(mm

)b

52

0.01

;r

52

0.01

P5

0.96

b5

0.62

;r

50.

62P

50.

00b

50.

22;

r5

0.18

P5

0.49

SHORTER COMMUNICATIONS 683

rapidly running streams, and the eggs of I. beddomiiare always located in shallow pools (approximately2 cm depth) away from streams. Several other speciesof frogs with semiterrestrial tadpoles from differentfamilies (Hoff et al., 1999) also are reported to breed inshallow pools or seeps of water away from the mainstream. Further, semiterrestrial tadpoles of thesespecies are also reported to have unusually longmuscular tails with low tail fins, pulmonary respira-tion, and tail-flipping locomotion (Hoff et al., 1999).Thus, morphological, physiological, and ecologicalconvergence is observed in semiterrestrial tadpolesregardless of their lineage. However, a need to jumpinto water before the rock surfaces dry may havefavored evolution of a large muscular tail to providethrust for movement by jumping before the actualemergence of limbs.

Acknowledgements.—The study was supported by agrant (SP/SO/C-29/2000) from the Department ofScience and Technology (DST), New Delhi, to SKS andpartly by UGC-SAP-II grant. DKV thanks Council ofScientific and Industrial Research (CSIR), New Delhi,for Senior Research Fellowship.

LITERATURE CITED

ALTIG, R., AND R. W. MCDIARMID. 1999. Body plan,development and morphology. In R. W. McDiar-mid and R. Altig (eds.), Tadpoles: The Biology ofAnuran Larvae, pp. 24–51. University of ChicagoPress, Chicago.

ANNANDALE, N. 1918. Some undescribed tadpoles fromthe hills of southern India. Records of the IndianMuseum 15:17–23.

HADDAD, C. F. B., AND C. P. A. PRADO. 2005.Reproductive modes in frogs and their unexpecteddiversity in the Atlantic Forest of Brazil. BioScience55:207–217.

HOFF, K. vS., AND R. J. WASSERSUG. 2000. Tadpoleslocomotion: axial movement and tail functions in alargely vertebraeless vertebrate. American Zoolo-gist 40:62–76.

HOFF, K. vS., A. R. BLAUSTEIN, R. C. MCDIARMID, AND R.ALTIG. 1999. Behavior: interactions and theirconsequences. In R. C. McDiarmid and R. Altig(eds.), Tadpoles: The Biology of Anuran Larvae,pp. 215–239. University of Chicago Press, Chicago.

JOHN-ALDER, H. B., AND P. J. MORIN. 1990. Effect oflarval density on jumping ability and stamina innewly metamorphosed Bufo woodhousii fowleri.Copeia 1990:856–860.

KURAMOTO, M., AND S. H. JOSHY. 2002. Tadpoles ofIndirana beddomii (Anura: Ranidae). Hamadryad27:71–77.

LANNOO, M. J., D. S. TOWNSEND, AND R. J. WASSERSUG.1987. Larval life in the leaves: arboreal tadpoletypes, with special attention to morphology,ecology, and behavior of the oophagous Osteophi-lus brunneus (Hylidae) larva. Fieldiana Zoology38:1–31.

SEMLITSCH, R. D., J. PICKLE, M. J. PARRIS, AND R. D. SAGE.1999. Jumping performance and short-term repeat-ability of newly metamorphosed hybrid and paren-tal Leopard Frogs (Rana sphenoecphala and Ranablairi). Canadian Journal of Zoology 77:748–754.

TEJEDO, M., R. D. SEMLITSCH, AND H. HOTZ. 2000a.Differential morphology and jumping perfor-mance of newly metamorphosed frogs of thehybridogenetic Rana esculenta complex. Journal ofHerpetology 34:201–210.

———. 2000b. Covariation of morphology and jumpingperformance in newly metamorphosed water frogs:effects of larval growth history. Copeia 2000:448–458.

WATKINS, T. B. 1997. The effect of metamorphosis onthe repeatability of maximal locomotor perfor-mance in the Pacific Tree Frog Hyla regilla. Journalof Experimental Biology 200:2663–2668.

WILSON, R. S., R. S. JAMES, AND I. A. JOHNSTON. 2000.Thermal acclimation of locomotor performance intadpoles and adults of the aquatic frog Xenopuslaevis. Journal of Comparative Physiology 170:117–124.

Accepted: 15 January 2009.

684 SHORTER COMMUNICATIONS