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*'' o 2002 by ch"i::i:1, ?:j:f l:".11'; Jj.l:"'' Shell Kinesis in Juvenile Desert , Gopherus agassizii Mlnsrn L. Mlnolnlr2

tDepartment of Biology, Calfornia State Ilniversitv, DomingueT Hills, Carson, Califurnia 90747 USA; 2Present Address: 5954 Sunfield Avenue, lnkewood, Califurnia 90712 USA I E-mai I : mm03 9602 @ student.fulle rt on. edu ]

Ansrnlcr. -Inarticulate active shell kinesis includes the ability of some and tortoises to reduce the size of the opening between the posterior margin of the carapace and the tips of the xiphiplastron by flexion without a hinge. This particular action pattern is designated posterior shell aperture reduction, or PSAR. When comparing mean percent kinetic PSAR capability of Gopherus agassizii neonates to juveniles and adults there is a significantrelationship between neonates(8.4Vo), juveniles (l2.5vo), and adults (2.4Vo). When G. agassizii neonates were pecked and prodded with a raven model, their mean PSAR capability increased from 8.4tol4.6%o. Kinetic PSAR is also significant in juveniles and adults of qreolatus (with a mean reduction of ll.2vo in juveniles), and marginally perceptible in comparably sized juveniles of scripta elegans (2.0Vo). As neonate and juvenile tortoises appear to have insufficient size or ossification to effectively protect them from large avian and carnivore predators, this inarticulate shell kinesis may protect the tail, soft tissues around the cloaca, and hind legs from smaller predators. But this action pattern could also be coincidental with general contractions of soft-bodied juveniles. Comparisons of juvenile G. agassizii with similarly sized juvenile T. s. elegans casts doubt on this alternative explanation; no comparable shell kinesis was evidenced in the latter species.

Krv Wonos.-Reptilia; Testudinesl Testudinidae, Gopherus agassizii;;Trachemys scripta elegansl tortoisel ; carapace; plastron; kinesis; hinges; behavior; predation

My observations in the field first prompted this study. In reduction, or PSAR. This motion reduces the posterior May 1995 a radiotelemetered juvenile desert exposure of the tail, cloaca, and hind legs by the adduction (Gopherus agassizii), 4 years old, was released from the Ft. downward of the proximate portion of carapace. While not Irwin, San Bernardino County, , USA, tortoise addressing the underlying anatomy of this defense mecha- hatchery - nursery exclosure (see Morafka et al., 1997).It nism, this paper will examine the ontogeny of the response. was observed to reduce the posterior shell aperture to nearly It will also evaluate the PSAR in simulated predation trials. complete closure when attacked by a raven. The raven was Previous literature (Bramble, 1 97 4;Bramble and Hutchison, unable to seize the shell, or grasp the hind limbs. Contraction 1981; Bramble et al, 1984) has often referred primarily to of the posterior shell aperture had completely obscured the active movement of shell components only by means of view of the posterior soft tissues. actual hinges (but see Pritchard, 1993). I will refer to any Chelonian shell hinges have often been assumed to shell movement, flexion or motion not dependent upon function as active defenses, contracted to protect body hinges, active or passive in its initiation, as inarticulate extremities against predation (Bramble, I9l4; Bramble and kinesis. Hutchison, 1981; Greene, 1988). Other manifestations of I tested the possibility that neonates reduce the posterior shell kinesis actively or passively involve discrete move- shell aperture and that the threat of a predator elicits a greater ment of both carapacial and plastral elements, often without reduction response. Specifically, I experimentally stimu- the demarcation of discrete externally visible hinges. Some lated neonate andjuvenile chelonians, of three taxa: Gopherus plastral kinesis may passively depress the xiphiplastron to agassizii, Homopus areolatl,ts, and Trachemys scripta accommodate deposition of larger eggs in adult female elegans, to assess their response for reduction of the poste- , G. berlandieri (Rose and Judd, 1991) and rior shell aperture. This study examines PSAR as an active some south Asian batagurids (Moll, 1985; Pritchard, 1993). reduction of the aperture in response to specific stimulation. Other examples of passive kinesis in the absence of hinge These experiments quantify the frequency and the degree of mechanisms are found in the flexibility of carapacial and aperture response in a range of age and size classes of G. plastral elements in which several very different patterns of agassizii. Further experiments test for aperture contractions skeletal modifications have evolved to accommodate wedging in comparable age or size classes among another testudinid into confined crevices, as illustrated by the , and an emydid turtle. Experiments were designed to test the Malacochersus tornieri (Ireland and Gans, 1972), and the following null hypotheses: 1) no aperture reduction in any Malayan softshell turtl e, Dogania subplana (Pritchard, 1993). group tested, 2) no difference between ages of G. agassizii, The voluntary shell closure being studied here is an 3) no difference between G. agassizii and H. areolatus, and active hingeless action designated as posterior shell aperture 4) no difference between G. agassilii and T. s. elegans. MnnolDA Shell Kinesrs 4tt -

Reduction of the posterior shell aperture mi_eht be Other test grollps were composed of individuals of randomly explained as an active defense if it were effective against mixed ori-eins as well. The first set of 32 captive hatched native predators within a natural habitat. Such predators in tortoises was challen-eed with the beak of a museum-pre- the native habitat of G. agassizii could include coyotes, pared raven in the following manner. Each tortoise was foxes, badgers, snakes, birds (especially ravens), and small placed upri-eht on a large flat surface and allowed to adjust rodents, arachnids, scorpions, and ants (U.S. Fish and Wild- to the surface until it was moving about normally and then life Service, 1994). While such an adaptationist explanation the posterior shell aperture was measured. The tortoise was is attractive, it must not be assumed without evidence of then tested in a simulated raven attack. The raven model was causation. Such assumptions led to the belief that the gopher moved over the tortoise to produce a shadow on the tortoise,, tortoise, G. polyphemus, excavated its burrow width as a which generally caused the tortoise to freeze in its position. purposeful accommodation of body size. In fact, burrow The raven was then placed in front of the tortoise and a width was demonstrated to be a simple function of G. pecking action was made with the beak against the anterior polyphemus forelimb positions in the excavation process, carapace. Neonates first responded pugnaciously with the for which no more adaptationist explanation was necessary "hatchling hop" (Berry, 1986) and then would withdraw or appropriate (Wilson et al., l99l). inside their shells, contracting to near closure. If a tortoise While it is uncertain how long the carapace and/or withdrew into its shell, the tortoise would then be turned plastron remains flexible, it is certain that juvenile chelo- plastron side up and the pecking motion was repeated on the nians are smaller, weaker, and morphologically more sus- posterior plastron. The posterior shell aperture was then ceptible to predation. Neonates (Morafka, 1994; Morafka et remeasured. Other neonates, juveniles, and adults of G. al., 2000) and juvenile tortoises will withdraw into their agassizii, juveniles and adults H. areolatus, and juveniles 7- shells, perhaps both enhancing crypsis and simultaneously .r. elegans were challenged with finger probing or a swab sheltering vulnerable extremities. In the case of small and using the same sequence of probes and turnovers as if the young tortoises vulnerability to small and mesopredators finger was the raven beak. becomes a particular issue (Greene, 1988; Morafka et al., Raven-threatened G. agassizii neonate CL was 40.5- 2000). Does the inarticulate kinesis phenomenon have adap- 52.6 mm. Finger-probed neonates aged 3 days to I month tive significance, is it an exaptation linked to some other had CL 44.9-51 .7 mm. Juveniles were 63.4-104.9 mm CL, physical function, or is it simply a muscular contraction in age 3-8 yrs. Adults ranged from 280 to 350 mm CL. Ages of response to being touched? all neonate and juvenile G. agassizii tortoises were known because they were either hatched in incubators at our labo- METHODS "ff :T T:,T ff [T:[i i3:: ;:i#', 3:T:iJ,:1# I T ; For this study I employed experimental methods to our predator resistant study'Yu site located on the Ft. Irwin elicit what appears to be a fixed action pattern using two National Training Center in San Bernardino Co., Cali- innate releasers (Starr, 1994): I ) a cotton swab and/or a fornia (see Morafka et al, 1991, for site and facility finger probe, and 2) a stuffed raven. All chelonians were description). measured along the midline carapace length (CL) from the posterior notch of the carapace to the nuchal notch to the nearest 0. I mm. The posterior shell aperture of each tortoise was measured to the nearest 0.1 mm from the pygal notch to the center of the anal notch (Fig. 1). Initially each tortoise was probed with a cotton-covered swab or finger probe near and about the rear legs and cloacal vent until a shell closing response was elicited. Each tortoise was then remeasured across the previously described coordinates to determine degree of reduction. The index of posterior shell aperture reduction (PSAR) for morphometric comparisons was ob- tained by the following equation:

minimum aperture 7o reduction PSAR - 1 x 100 - maximum aperture

Thirty-two naive G. agassizii neonates (in the sense of Morafka, 2002) were challenged. They were all hatched from eggs of captive tortoises provided by Southern Califor- nia Chapters of the California Turtle and Tortoise Clubs. Figure 1. Area of posterior shell aperture showing the relaxed They were derived from approximately six clutches of eggs position (left) and a contracted aperture (right) in G. agassizii, demonstrating the measurement of the aperture opening (b) in the and randomly assigned to experimental groups to reduce two positions, with the difference (in percent) defined as the clutch-specific effects on physical condition or behavior. posterior shell aperture reduction (PSAR). 412 CusloNrnN CoNSERVATToN AND Btotocv, Volume 4, Number 2 - 2002

Neonate Trachemys scripta elegans were purchased 18.00 : Fsrimulus=9'781 P=0'00'31 from Thibodaux Live Supplies of Louisiana where they 16.00 : were supposedly hatched in their natural environment. Neo- : natal Z. s. elegans were 34.8-37 .2mmCL, age2 wks - I mo; 14.00 i juveniles had CL92.l -99.0 ffiffi, and were estimated to be 4- r z.oo i 7 yrs. I compared G. agassizii finger-probed neonates to G. () agassizii juveniles and Z. s. elegans neonates and juveniles 10.00 C, using sets in comparing CL groups to see if there was a & ()u 8.00 difference between families. a) A. Homopus areolatus were provided by the West Cape 6.00 Province Wildlife Commission, South Africa. They were maintained in planted and fenced outdoor pens in Los 4.00

Angeles prior to measurement. Juveniles were 51.8-72.2 2.0n mm CL, and adults had CL 93.0-1 13.2 mm. 0.00 Finger Prohe Raven Threat RESULTS Figure 2. Histogram of percent of posterior shell aperture reduc- tion (PSAR) of G. agassizii neonates showing response to finger probes for finger probe is * I .46, Those G. agassizii neonates that were challenged by a and to raven model. Standard error raven model demonstrated the greatest percent PSAR (mean 14.6Vo). groups The remaining are listed by their diminish- 16.00 T I Gopherus agassizii Fspecies 91.3g4 p < O.OOO! i = L ing responses: G. agassizii juveniles (I2.57o), H. areolatus Trachemys t scripta Fsize = 13.595 p = 0.0004 juveniles (II.2Vo), G. agassizii non-raven threatened neo- 14.00 nates (8.47o),7.,s. elegans neonates (5.4Vo), H. areolatus 12.00 adults (5.2Vo), G. agassilii adults (2.4Vo), and Z. s. elegans juveniles (2.0Vo).In all tests where PSAR was observed, it 10.00 was measurable even when the head and hind limbs had (., ! c) already been retracted, and was not simply incidental to & 8.00 those defensive movements. ou o o- The diagram in Fig. 2 compares finger probes vs. 6.00 raven model in stimulating PSAR. Given the raven threat, 4.00 neonate tortoises (n = 32) reduced the posterior shell t I aperture more (mean 14.6Vo) than those G. agassizii (n - ?,aa 14, mean 8 .47o) merely probed with a finger or touched 0.00 i with a swab. ANOVA arcsine was F = 9.781 and p = I Ne

. 250 mm CL. Figure 4 demonstrates that for species compari- 2.00 - sons F - 196.057 and p < 0.0001 , and that for size compari- sons F - 18.564 and p < 0.0001. Note in Fig. 4thatthere is 0.00 --- - - I Juvenile 2 Adult a small difference betweenjuvenile G. agassizii andjuvenile H. areolatus (n = 4, mean 1 I .2), aminor difference between Figure 4, Acomparison of PSAR in experimental trials ofjuvenile and adult G. agassi:ii and H. areolatus. Standard errors are as adult G. agassizii (n 6, mean2.4) and adult H. areolatus (n = follows: + 0.92 for juvenile and * 0.89 for adultG. agassizii;+ 3.56 = 8, mean 5.2).However, there is a significant level of for juvenile and * 0.99 for adult H. areolatus. MnnolDA Shell Kinesis - 4r3

produced a 2.0Vo mean, statistically an effectively negative 14.00 ri response to aperture reduction. F=49.251 P<0.0001 i

l 12.00 I also compared different age-srze classes among G. ' agassizii, examining the role of ontogenetic changes as

10.00 - inferred by CL. Comparing the neonates to juveniles to adults by ANOVA arcsine, &S shown in Fig. 6, juveniles manifest significantly greater percent PSAR (F = 7 .1I5, p = 0.0017).

DISCUSSION

Active shell kinesis of parts of the carapace and plastron are common in small-sized species of chelonians (but see Pritchard, 1993). If such kineses are generally associated with small srze,, they may be a fundamental .t q 3 characteristic of t1 w, .$ {i j\ young tortoises (Richmond, 1964). Thus, an adaptive expla- s S.) 3 ? nation of PSAR could prove unnecessary if it is just an si q, $ 'J expression of the flexibility of small, poorly ossified shells. 3 t _t \ However, active inarticulate kinesis does not appear to be a simple function of size, as it is not found in all young turtles Figure 5. Comparison of PSAR of samples of juveniles G. of and tortoises, as illustrated by the results of tests of T. .r. agassizii, H. areolatus, and T. .r. elegans in response to finger elegans in this study. probing. Standard errors are + 0.92 for G agassiTii,+ 3.56 for u. Further, adult G. agassizii have little areolatrus, and + 0.92 for 7'. s. elegans. kinetic ability to reduce the posterior shell aperture, even when adult females may manifest the passive depression of the xiphiplastron previously cited for G. berlandieri. How- ever, the reverse is manifest in the ontogeny in the passive

carapacial kineses. For the pancake tortoise , (Malacochersus tornierl) (Obst, 1988) and the Malayan softshell rurrle, Dogania subplana, flexibility is most evident in adults (Pritchard, 1993). ,J Data from field studies confirm the special vulnerability lc} c) g, of young tortoises to predation. Wilson (1994) noted that of q)tr U eleven subadultG. polyphemus found dead on her study plot, () F. three showed evidence of predation by raptors, and the other eight seemed to have been eaten by mammals as their shells were torn apart in a manner indicative of mammalian preda- tion. This was 347o out of a total of 32 radiotagged juvenile tortoises during one year of study. Morafka et al. (I99i) indicated that 18 of 24 (l5Vo) G. agassizii juveniles in an unroofed enclosure were lost to avian predators, and that 8 Figure 6. The ontogenetic cohort testing of G. agassizii of of 1 2 (61Vo) free-ranging radiotransmittered juveniles were neonates, juveniles, and adults for differences in PSAR. Standard similarly preyed effors are * L.46 for neonates, + 0.92 for juveniles, and * 0.89 for upon. Additionally, Morafka (I99i) re- adults. ported that 3- and 4-y, old desert tortoises were released from their enclosure and only 66.7Vo survived. In contrast, difference between the juvenile and adult cohorts. Compar- total annual mortality for adult G. agassizii has been shown ing juveniles and adults of both species by ANOVA arcsine to be as low as about2Vo (Berry and Turner, 1986). demonstrated thatjuveniles were more capable of reduction There is considerable variation in the length of time that than adults in both species. Therefore, although this phe- the plastron and carapace of desert tortoises remain soft. nomenon is not entirely restricted to juveniles, its strongest Ossification of the shell may be insufficient to provide manifestation is in the juvenile cohort. resistance to predators for up to 7 yrs (Morafka, I99l). I repeated the study using ANOVA arcsine forjuveniles Luckenbach (1982), Appleton (1986), Adest er al. (1989b), of T. s. elegans. The results, displayed in Fig. 5, comparing and Morafka ( 1994) indicated that the plasrra in borh G. samples of juveniles of different species show that the flavomarginatus and G. agassizii remained relatively soft terrestrial testudinid species were more capable of PSAR for 5-10 yrs. than the one aquatic emydid (F = 49.251, p Neonate and juvenile shells have been Gopherus agassizii juveniles had al2.57o mean, H. areolatus found at raven nesting sites with holes punctured in the had slightly less with an 1 l.2Vo mean, and i". s. elegans tests carapace or plastron (Boarman, 1993; Morafka et al., 199j). 414 CHEI-oNteN CoNSERVATToN AND BroLocv, Volume 4, Number 2 - 2002

Ravens may also scavenge tortoise carcasses from other length with the incidence of kinesis is not universal to all predators, or may obtain the remains of recent deaths due to young chelonians, virtually absent in the generahzed and disease or dehydration. High raven densities may be rela- presumably representative juvenile Ls. elegans, and 3) tively new to the Mojave Desert (Boarman, 1993). There- PSAR is an active adduction of the posterior carapace, not fore, the long term roles of other tortoise predators might be simply a passive flexor in response to extreme pressure, or overlooked, especially those of non-passerine avian preda- a motion coincidental with hind limb contraction. tors, as well as canids, small cats, some mustelids such as This study has confirmed that neonate and juvenil e G. badgers (Taxidea taxus), and many viverrids. In California agassilii can actively reduce the posterior shell aperture. deserts juvenile tortoise carcasses have been found in asso- However, future studies need to determine the anatomical ciation with nests and perches of eagle, Aquila chryaetos, mechanism involved in this reduction phenomenon, the role roadrunner , Geococcyx californicus, hawk, Buteo of crypsis in hatchling predator/prey relations, and as well to jamaicensis, and owl , Athene cunicularia (Boarman, identify predators that would be deterred by PSAR. This 1993). Kinesis (PSAR) may be most effective for juve- phenomenon also needs to be examined in G. agassiziiof CL niles where the carapace had hardened somewhat but the between 100-200 ffiffi, other Gopherus species, and a thor- plastron was still slightly soft. Smaller avian predators ough survey of other testudinids. such as shrikes, jays (Green e,1988), buteos, and accipitors would be unable to readily penetrate the carapace or gain AcxxowLEDGMENTS access to the soft plastron unless they could overturn the tortoise. Although the benefits of PSAR are potenrially I thank D.J. Morafka for suggesting this investigation greater in young tortoises because of their obvious vulner- and for many useful discussions of the phenomenon, as well ability, the overall effectiveness of shell kinesis for predator as moral support and guidance in the writing of this paper. I protection remains to be established, possibly in arenas also thank D. Hadley for the tortoise illustrations; W. Alley where captive prey-predator encounters may be stereotyped for assistance with the statistical analysis and graphs; and D. and quantified, perhaps following a methodology adopted Richards for her data on exotic species compiled in 1981 . from Okamoto (2002). This study was funded by contracts awarded to D.J. Morafka Reduction may be effective against smaller mammalian by So. California Edison, world wildlife Fund, and the predators that gnaw, such as insectivores and rodents. Grass- Directorate of Public Works (DPW) of the U.S. Army hopper mice (Onychomys torridus) might use tortoises as a National Training Center at Ft. Irwin, California. I am rich source of protein. Tail and hind limbs might also be particularly appreciative of the continued support of M. protected from attacks from large predatory arthropods, Quillman, Natural and Cultural Resources Director, DPW, such as scorpions and beetles. Such mechanical protection Ft. Irwin. as PSAR however, would not provide protection against very small arthropods, such as mosquitoes, ticks, flies, ants, LITERATURE CITED or any other known insects. Likewise PSAR would afford no Anesr, G.A., Acurnns L., G., Monnpre, D.J., AND protection against very large predators, like canids, which JnncHow, J.V. I 9 89 a. B ol s on tortoi se (G o p h e ru s av o ma r g inatus) con serv ati on : could swallow young tortoises whole. fl I. Life history. Vida Silvestre Neotrop .2(l):7-13. Several alternative functional consequences ofj uvenile AoESr, G.A., Acurnne L., G., Monepra, D.J., AND JancHow, J.V. shell kinesis in tortoises may be considered. Could it be for I 9 8 s (G 9b. B ol on tortoi se o p he ru s fI av o ma r g inarrzs) c on serv ati on : conservation of water; that is to prevent water loss in an arid II. Husbandry and reintroduction. Vida Silvesffe Neoffop .2(l):14-20. environment? If that were the case the PSAR would be Appr-EroN, A. 1986. Furtherobservations of Bolson tortoises (Gopherus evident when the tortoise was at rest. Reduction is a definite flavomarginatus) at the Appleton-Whittell Research Ranch. Desert motion of actively drawing the carapace down and, as a Tortoise Council, Proceedings of the 1983 Symposium, pp. 108- ll4. BERRY, K.H. 1976.4 response to touch, an active depression. Might it be an comparison of size classes and sex ratios in four populations of the desert tortoise. Desert Tortoise Council, Pro- ontogenetic precursor to female xiphiplastral hinging de- ceedings of the 1976 Symposium, pp.38-50. scribed by Rose and Judd (1991) to enlarge rhe posterior BEnRy, K.H. l98l . State report - California. Desert Tortoise Council shell aperture for egg deposition? Or is this manifestation a Proceedings 198 I Symposium, pp. 49-52. non-functional byproduct of muscle contraction on a poorly BennY, K.H. 1986. Desert tortoise (Gopherus agassizii) relocation: calcified shell? Indeed, Ernst and Barbour (1989) recog- implications of social behavior and movements. Herpetologica nized greater flexibility of young tortoise shells, which 42(r): I l3- 125. might predispose such individuals to more general body BERRy, K.H. AND Nrcsor-sol, L.L. 1984. Attributes of populations at contractions when they were probed. The responsive nature twenty-seven sites in California. In: Berry, K.H. (Ed.). The status of the desert (GopherLrs of inarticulate kinesis in juvenile tortoises suggests that it is tortoise agctssizii) in the United States. Report to U.S. Fish and Wildlife Service from the Desert Tortoise an active protective manifestation, rather than a coincidental Council on Order No. I l3 10-0083-81, pp. 154-241. biproduct of general body movements or contraction. This BEnnY, K.H. AND TunNEn. F.B. 1986. Spring activities and habits of conclusion is supported by three observations: 1) an innate j uvenile desert tortoi se s. G o p lt e rus a g as s i zii, inCaliforni a. 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