Paradoxical Reproduction and Body Size in the Rock Lizard, Agama Atra Atra, in Namaqualand'south Africa

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provided by Stellenbosch University SUNScholar Repository http://africanzoology.journals.ac.za S.Afr. J. 2ooL1994.29(J) 199 Paradoxical reproduction and body size in the rock lizard, Agama atra atra, in Namaqualand'South Africa

P.le F.N.Mouton" J.EllermanMuseum, Department ol Zoology,University of Stellenbosch,Stellenbosch, 7600 Republic of SouthAlrica Y.M.Herselman Departmentof Anatomyand Histology,University of Stellenbosch,Tygerberg, 7507 Republic of SouthAfrica

Received5 July 1993;accepted Il February1994

The rock lizard Agama atra atra from Namaqualanddiffers in both body size and reproductionfrom other populationsof this speciesoccurring elsewhere in southernAfrica. Both sexes from Namaqualandare significantlylarger than their counterpartsin the south-westernCape. While reproductionin this speciesis stionglyseasonal elsewhere, it is apparentlycontinuous in Namaqualand.Females with vitellogenicovarian follicle6and/or oviducal eggs were collectedduring the winter monlhs,a time when femalesare typically reproductivelyquiescent in otherpopulatlons. Aseasonal reproduction and largebody size ol this speciesin Nimaqualani do not correlatewith prevailingenvironmental condilions in the area.The presenceol at least one other specieswith continuousreproduction and two otherswith tropicalaifinities in the same general area,suggests that the Namaqualandpopulation of A. a. atra maybe a tropicalrelict.

Die bloukopkoggelmander,Agamaatra atra,wat in Namakwalandvoorkom, verskil in beide liggaamsgrootte en voortplantingvan anderpopulasies van hierdiespesie wat eldersin suidelikeAf rika aangetrefword. Beide geslagtevan die Namakwaiandsevorm is aansienlikgroter as hul eweknieiielders. Voortplanting by hierdie in Namakwalandis dit oiinskynlikaaneenlopend. Wylies met ipesie is eldersuitgesproke seisoenaal, maar 'n vitellogenetiesefollikels en/of eiers in die ovidukte,is gedurendedie wintermaandehier versamel, tyd van 'n die jalr wanneerwyfies tipies in reproduktieweruslase verkeer in ander populasies.Aaneenlopende voortplantingen groot liggaamsgroottevan hierdiespesie in Namakwalandkorreleer nie met heersende omgewingstoestandein die gebied nie. Die teenwoordigheidvan ten minste een ander spesie met aarieenlo-pendevoortplanting en twee ander met tropieseverwantskappe in dieselfdealgemene gebied, dui 'n daaroodat die Namakwalandpopulasie van A. a. alramoontlik tropieseoorblylsel mag wees.

* To whom correspondcncc should be addressed

Reproduction in reptiles is generally closely co-ordinatcd southernNatal (Fitz-Simons1943; Branch 1988a).An isola- with the environment(Fitch 1970;James & Shine 1985).In ted population also occurs on the Transvaal escarpment temperatc zone forms, reproduction is typically seasonal (Branch 1988a;Jacobsen 1989). This speciesis a diurnal with distinct periods of activity followcd by pcriods of oviparouslizard which inhabits rocky areas,from sea level quiescence(Fitch 1970;Heatwolc 1976;Fox 1977;Duvall, to high elevation(* 2000 m above sealevel). Two racesare Guillette & Jones 1982). Various patternsof seasonalor recognizedbut thcse are poorly delimited (Branch 1988b). discontinousreproductive activity havc bcen rclnrted, thc The typical race, A. a. ota, has an extensive range in mostcommon being that in which malesand femalesexhibit southern Africa, whereas A. a. knobel/i is restricted to spring gonadogenesis,followcd by courtship,mating and southernNamibia (Branch 1988a). ovipositionfitch 1970; Duvall et al. 1982; Ficht 1984; As is typical of tcmperate zone oviparous forms, A. a. & Lofts 1985; Mendez de la Cruz-,Guillette, Santa Cruz alrc exhibitsspring gonadogenesisover most of its range Mendezde la Cruz 1993). Casas-Andrew1988; Guillette & (Van Wyk 1983;Branch 1988a;Jacobsen 1989; Mouton & pattem is especially dorninant The lattcr discontinuous Van Wyk 1993; Flemming pers. comm.). Recentsurveys, species(Fitch 1970).In tropicalforms, on amongoviparous however,revealed that A. a. atra from Namaqualandin the the other hand, reproductionis often aseasonalor contt- Cape Province(Figure l) is not only apparentlymuch largcr nuous,although many forms exhibit cyclical reproductive in body size, but.is reproductivecycle also differs substan- patterns 1970;Shcrbrookc 1975; Guillette & Mcndcz @itch tially from that recorded for this species elsewhere in dc la Cruz 1993). southernAfrica. We providc preliminary data demonstratlng Thc agamidsare a diversefamily of Old World lizards the paradoxial nature of body size and reproduction in often regarded as the counterparts of the New World NamaqualandA. a. atra and briefly discussthe implications iguanids.Nearly all are oviparousand most agamasstudied of our obscrvations. to date show a well defined breeding season,even in the tropics(Fitch 1970;Van Wyk 1983;James & Shine 1985; Materialand Methods Jacobsen 1989; Heideman 1992; Mouton & Van Wyk 1993).The southernrock agama,Agama clrc Daudin 1802, Dunng 1992several localrties in Namaqualandwere visited is a medium sized southcm African lizard which occurs from which specimensof A. a. atra were collected(Figure throughout the Cape Province, Orange Frec State, south- 1). Other matcrial from various localities in the south- westernTransvaal, southem Namibia, Lcsotho, Transkei and westernCape, excluding Namaqualand(Figure l), was also http://africanzoology.journals.ac.za 200 S.-Afr. Tydskr. Dierk. 1994,29(l)

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Figure 1 L-ocalities in Namaqualand from which Agama atra atra TIME OF YEAR

of large body siz-c and with apparent continuous reproduction, postovutotory ff Postoviposition @ were collected (shaded circles). Major towns in the area are $ Eorly vitellogenic El Lote posrovutorory represented by open circles. The ,100 m and 1ff)0 preovulotory m contours are ffi shaded. The area in the south-western Cape from whcrc additional material was examined, is also indicated. Figure 2 Stackcd bar diagramsshowing the percentageof females of Agama atra alra in the various reproductivestages at different times of the year for (a) Namaqualandand (b) the south-wesrem examinedto determincdifferenccs in body sizc and timing Cape [see Van Wyk (i983) for a full descriptionof the stages] of reproductiveevents among t.heNarnaqualand and south- Thc monthly samplc sizesappear above the bars. wcstcrnCape populations.All rnatcrialused in this study is housed in tie Ellerman Muscum of thc University ol' Stcllcnbosch. males and femalcs from the two regions were compared Snout-vcntlength (SVL) was mcasuredfrom preservcd separatcly. specimens to the nearest.0, I mm using digital vernier calipers.The right ovary and oviduct of all femalcswere Results removcdand the meandiameter of the threelargest folliclcs The reproductive stagesof female A. a. atra collectedin in each ovary measurcdto the nearcst0,01 mm. The repro- Namaqualandare listed in Figure 2a. Data were available ductivestagcs proposed by Van Wyk (19tt3)for A. a. atra only for lhc months May, July, Septemberand December. wcre used to qualitativelydescribe the rcproductivccondi- During all four months gravid females(with oviducaleggs) tion of the females(Figure 2). The righr tesrisof all malcs or femalcswith vitellogenicovarian follicles were presentin examincdwas removcd. The longcstand shortcstaxes of thc the samplcs. During carly Septemberall five reproductive testcswere measurcdto the ncarcst0,01 mm. Testicular stages were recorded among the fcmales examined. In volumc was calculatcdas being cllipsoid.Paraffin sections oonlrast,all lhe south-westernCape femalescollected during (4-7 pm) were raken from the middle of the tcstes and the period Fcbruary to June (n = 17) were reproductively stainedwith hematoxylinand eosin.Spermatogcnic activity quiescent"i.e. with hydration stage follicles and without wasassessed using the classificationof Licht (1961). oviducal eggs (Figure 2b). All south-westernCape females The Mann-WhitneyU test(Zar 1984)was usedro resrfor (n = 19) collectcd during the period mid-July to mid-January significant differences in body sizc betwecn animals were reproductively active, displaying either vitellogenic collectedin Namaqualandand thosccollected clsewherc in follicles or oviducal eggs (Figure 2b). Vitellogenesisstafls thc south-westcrnCape (/, < 0,05 consideredas significant). from late July to early August, with ovulation occuning Owing to considerablcscxual dimorphism in krdy size, from mid-Scptcmberonwards. Females with oviducal eggs http://africanzoology.journals.ac.za S.Afr. J. 7nol. 1994,29(3) 201 were collectcdfrom mid-Septcmberuntil mid-January,but not later. Data for Namaqualandmales wcre availablc only for thc months April, May, July, Scptemberand Decembcr.Testi- cular volume remained fairly constant during this pcriod figure 3a), while histological cxamination showed that spermatidsand spermatozoawerc abundantin the semini- fcrous tubulcs of males collectcd dunng these months (Figure 4a). South-wesLcrnCape males, in cont-rast,showcd a distinct period of testicular regrcssion from the end of January until April, as is evident liom a dscrease in tcsticular volume (Figure 3b). Histological examination showedthat during this pcriod the scminiferoustubules are involuted with only sperrnatogoniapresent (Figure 4b). Towards the end of April an abrupt incrcase in testicular volume is evident in south-westernCape males (Figure 3b). l-"{ From this time onwards until mid-January,both spermatids and spermatozoaare prescnt.in the seminiferoustubules. The body size (SVL) distributionof lemale and male samplesol A. a. atra from Namaqualandand the south- westcrnCape is shown in Figure 5a and 5b, respectively. Thc Mann-Whitney U test showcd that both malcs and fcmalescollected in Namaqualandattain significantly larger body sizes than males and fcmales collccted elscwhcre in thesouth-wcstern Cape (p < 0,05). The rangeof the largeNamaqualand agama with apparcnt

Figure 4 Crosssections through the testesof Agann atrd alra males:(a) collectedin Namaqualandat the beginningof April' showing seminiferoustubules with spermatidsas well as

I spermatozoa,(b) collectedin the south-westernCape during r;- with only. F r

b: Southwestern Cope 1989;Mouton & Van Wyk 1993;Flcmming, pers. comm.). Furthcrmore, thc timing of reproductive events among JFMAMJJASOND femalesprcscnt at any lmality is normally well synchro- TIME CF YEAR nizcd. The trming of events also seems to be remarkably l-igure 3 Scattcrplotsof testicularvolume againsttime ol the year conservative geographically as no significant differences for Agama atra atra males from (a) Namaqualandand (b) the were noted among populations as far apart as the south- south-westernCape. westernCape, Transvaal, Orange Free Stateand the Lesotho http://africanzoology.journals.ac.za 202 S.-Afr.Tydskr. Dierk. 1994,29(3)

Food availability is an important determinant of life o: Femoles history attributes such as body size and reproductive effort (Case 1978; Schwaner1985; Plummer 1981;Peters 1983; Brown, Marquet & Taper 1993). The relarionshipbetween body size and allocation of energy to reproductionis also d10 well documented (see, e.g. Harvey, Read & Promislow z 1989;Reiss 1989; l Chamov 1991).Thus in remperateareas with seasonalclimates, where resources may E be limited L during certain times of the year,reproduction would typically be discontinuousfitch 1970; James & Shine 1985; Guillette & Mendez de la Cruz 1993).Furthermore, in order to maintain the required reproductive output, less energy may be invested in growth in temperateareas (see, e.g. Firch 1978).The climate in Namaqualand,as elsewherewittrin the range of A. a. atra is seasonal(Schulze & McGee 1978). Steep gradienl.sin most.climatic paramatersoccur from the coast to the interior so that.A. a. atra is here subjectedto a broad range of environmentalconditions. That A. a. atra 'tropical' should display life history attributesin this tem- > 1n z peratearca is Lhereforcsurprising. :) o Thcre are two possible explanationsfor the paradoxical

L body size and reproductionof A. a. atra in Namaqualand and clues in this regard are provided by other speciesin the area.Firstly, Goldberg & Robinson (1979) reporredlhar reproduction in the lacertid lizard Meroles anchietae,occurring in the Namib Desert,is also aseasonal.They concluded that the perennial availability of windblown seedsallows

60 E0 100 120 140 this omnivorous speciesto obtain enough energy for year- round producrion.The possibility thus exists in SVL(mm) that the case of A. a. otra some unknown environmental factor may I Nomoquolond SouthwesternCope @ directly or indirectly influence food availability resultingin Figure 5 Frequency histograms showing differences in size an all-year-roundsupply. Secondly,at least two lizard spe- classes bctween Namaqualand and south-wcstcrn Cape popula- cies with tropical affinities are endemic to the Namaqualand tions of Agama atra atra, for (a) females and (b) males. area. The Namaqua day gecko, Phelsuma ocellata is the only speciesof this tropical genus occurring on the main- land of Africa; the otier + 25 speciesoccurring on Mada- Highlands(Van Wyk 1983;Jacobsen 1989; Mouron & Van gascarand other tropical islandsin the Indian Ocean(Welch Wyk 1993; Flemming, pers. comm.). Dara presenred here, 1982).Thc Cape flat liz,ard,Plarysaurus capensis is the only however, show that the female rcproductive cycle A. of a. speciesin the gcnus presentin the westernparts of southem atra in Namaqualanddiffers from the fcmale cyclc recorded Africa, the other 1l species occurring in the subtropical elsewhere in South Africa in that reproductive activity north-easternparts of the southern subcontinent(Broadley apparently does not cease during the autumn and winter 1966;Branch 1988a).The presenceo[ thesetwo speciesin months.Furthermore, unlike elsewhere,the riming of rcpro- the same generalarea as the large agama suggcststhat they ductive events seems to be poorly synchronizedamong may all share the same biogeographicalhistory, i.e. they females. may be tropical leftoversin what is now a temperateregion. Resultsobtained in this study for south-westernCape A. a. atra, as well as dan availablefor other regions(Jacobsen Acknowledgements 1989; Mouton & Van Wyk 1993; Van Wyk, unpublished We thank A.J. Lintvelt, I.G. Cordes,H. Geerrsema(Jr) and data for Orange Free State), suggestthat male reproductive A.M. Bauer for assistancewith fieldwork; A.F. Flemming activity, typical of temperatezone oviparousspecies, is also for commentsand additional information; J.A.J. Nel for the seasonalover the greaterpart of the range.Lack of data for opportunity to accompanyhim to the Vaalputsarea; and H. the months February and March, the period when testicular Geertsema(Sr) and M.H.C. Visser for the critical readinsof regressionis particularly evident elscwherewithin the range the manuscript. of this species@igure 3b), does not allow definite conclu- sions to be reachedregarding reproductivc activity in male References A. a. ato from Namaqualand.Nevertheless, the presenceof only reproductivelyactive males in a samplccollected at the BRANCH, W.R. 1988a.Field guide ro snakesand orher reptiles beginningof April (Figures 3 & 4), indicaresthe possibility of southernAfrica. Struik Publishers,Cape Town. that in Namaqualand,males may be reproductivelyactive BRANCH, W.R. (ed.).1988b. A provisionaland annotared throughoutthe year. More detailed investigationsare, how- checklistof the herpetofaunaof southernAfrica. J. Herpetol. ever,needed to confirm this. Assoc.Afr.34: l-19. http://africanzoology.journals.ac.za S.Air. J. 7nol. ).994,29(3) 203

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