Journal of Threatened Taxa | www.threatenedtaxa.org | 26 June 2023 | 15(6): 23307–23314

 

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) 

https://doi.org/10.11609/jott.8473.15.6.23307-23314

#8473 | Received 07 April 2023 | Finally accepted 21 May 2023

 

 

Plastral deossification zones in the Endangered Spiny Hill Turtle Heosemys spinosa (Testudines: Geoemydidae) on Borneo

 

Siti Nor Baizurah 1  & Indraneil Das 2

 

1,2 Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia.

1 sitinorbaizurahabdulmalik@gmail.com, 2 idas@unimas.my (corresponding author)

 

 

Editor: Raju Vyas, Vadodara, Gujarat, India.                   Date of publication: 26 June 2023 (online & print)

 

Citation: Baizurah, S.N. & I. Das (2023). Plastral deossification zones in the Endangered Spiny Hill Turtle Heosemys spinosa (Testudines: Geoemydidae) on Borneo. Journal of Threatened Taxa 15(6): 23307–23314. https://doi.org/10.11609/jott.8473.15.6.23307-23314

 

Copyright: © Baizurah & Das 2023. Creative Commons Attribution 4.0 International License.  JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

 

Funding: Niche Research Grant from the Ministry of Higher Education, Government of Malaysia (NRGS/1087/2013(01)).  Research permit: Sarawak Forest Department, for issuing the permit (No. 181/JHS/NCCD/600–7/2/107; Park Permit No. WL 88/2018)

 

Competing interests: The authors declare no competing interests.

 

Author details: Siti Nor Baizurah is a PhD graduate from UNIMAS, previously worked on the herpetofauna ecology for her postgraduate studies and her research interests include ecology, anthropogenic effects on ecosystem, human wildlife conflicts and wildlife management.  Indraneil Das received a D.Phil in Zoology from the University of Oxford, and was a Fulbright Fellow at Harvard University. He is currently professor at the Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, where he conducts research on the systematics and ecology of the herpetofauna of Borneo and south-east Asia.

 

Author contributions: SNB carried out the research work, providing data (ie: photographs, measurements) and drafted the manuscripts. ID coordinated the data and participate in writing and reviewing the manuscript. All author agreed to the final version.

 

Acknowledgements: This project was funded by a grant under the Niche Research Grant Scheme (NRGS), awarded by the Ministry of Higher Education, Government of Malaysia (NRGS/1087/2013(01) and a Conservation Leadership Programme (CLP) Grant. Our deepest gratitude goes to our veterinarian, Davies Belayong and his colleagues at the Animal Veterinary Clinic Kuching for assisting with radiography. We would like to acknowledge the Institute of Biodiversity and Environmental Conservation, UNIMAS for providing facilities and equipment, and would like to single out Andrew Alek Tuen, Gabriel Tonga Noweg and Rahah binti Mohamad Yaakup, and the Research, Innovation and Enterprise Centre under Lo May Chiun for managing the NRGS project. The research undertaken and animal handling procedures used in this work were approved under permits issued by the Sarawak Forest Department (No: 181/JHS/NCCD/600–7/2/107; Park Permit No: WL 88/2018). Finally, we thank our friends in IBEC, Izneil Nashriq, Anthony Pine, Veronica Martin and Wong Jye Wen for assistance with field work, and the staff of Sarawak Forestry Cooperation at Kubah National Park for permitting access to the study site, particularly, Stephen Antang and Siti Wahdaniyah.

 

 

Abstract: Studies of the evolution of turtle shell morphology have raised numerous questions. In this study, five adult females and two adult males of the Endangered Spiny Hill Turtle Heosemys spinosa from two localities in western Sarawak in East Malaysia (Borneo) were examined for the presence of plastral deossification zones, reported as indicative of kinesis in earlier studies. A total of 52 (34 females, 18 males) radiographs demonstrated distinct poorly-ossified areas across the hyo-hypoplastral and the hypo-xiphiplastral junctures in females of straight carapace length (SCL) 143.4–211.4 mm. The feature is here interpreted as a permanent plastral hinge, which was not observed in either of the males examined. The smallest female with a weak but discernible line at the contact of these bones had a SCL of 125 mm, suggestive of minimum size of maturity in Heosemys spinosa in this population.

 

Keywords: Biology, growth, maturity, osteology, plastron, reproductive biology, sulcus, turtle.

 

 

 

INTRODUCTION

 

Evolution of turtles has produced variations in shell morphology and pelvic elements (Rivera 2008; Williams & Stayton 2019) and shell kinesis, although female plastral kinesis remains speculative in most species. The degree of kinesis depend on specializations in muscle and ligament systems, and active kinesis usually involves  modifications of kinetic structures that allow flexibility through voluntary muscle connections (Pritchard 2003). In passive kinesis, modifications of muscles are not necessary and may rely on pressures exerted over certain periods, including for respiration. For instance, pelvic kinesis in Homopus signatus (Hofmeyr et al. 2005), posterior plastral lobe kinesis in Heosemys spinosa (Mertens 1942, 1971), carapacial pankinesis in Dogania subplana (Pritchard 1993) and Kinixys erosa (Pritchard 2008) have been assumed on the basis of structure, although their mechanism and function is poorly known. Shell kinesis has been reported in smaller individuals of terrestrial or semi-terrestrial species as a possible adaptation to escape predation and aid locomotion (Berlant & Stayton 2017; Cordero et al. 2018). In contrast, posterior plastral lobe kinesis reported in H. spinosa has been hypothesized to be part of its reproductive strategy (Waagen 1984; Moll 1985), even though the shell was once considered as akinetic, and the possibility of plastral muscle specialization has been proposed (Bramble 1974). The hinge in H. spinosa reportedly develops in mature females (Moll 1985), resembling the hinge position displayed in the genus Cuora, albeit the kinesis in H. spinosa is limited to the posterior part of the plastron (Pritchard 1993).

Shell kinesis harbours numerous advantages, including predation survival, locomotion and facilitation of the passage of large eggs in small turtles. Accordingly, variation in the turtle shell has been speculated to be affected by multiple pressures, including phylogenetic, environmental and reproduction, in which plastral kinesis is one result of those pressures (Angielczyk et al. 2011). It is important to note that plastral modifications is usually expressed strongly in adults of both sexes in kinetic species (Ernst & Barbour 1989). Consequently, a number of studies (reviewed in Cordero & Quinteros 2015) discusses the adaptations of shell kinesis to habitat preferences, while sexually dimorphic kinesis must be related to reproduction strategy benefits, although a recent study suggests that the evolutionary structure of shell kinesis may stem from more complex relationships between ecological, phylogeny, and developmental processes in turtles (Cordero et al. 2018).

In the present study, we examine adults of the Spiny Hill Turtle from two free-ranging populations in Sarawak, East Malaysia (northwestern Borneo), in order to understand plastral kinesis (represented by plastral sulcus). Specifically, we will try to ascertain if the feature is restricted to females, the specific plastral bones associated with sulcus, the minimal size of animal that correlates with the development of the feature, and finally, if there are seasonality in variation of the feature.

 

 

MATERIALS AND METHODS

 

Data on plastral morphology were collected within a larger study on the spatial and thermal ecology of the Spiny Hill Turtle from two localities in western Sarawak, northern Borneo. The first was from Kubah National Park (headquarters at 1.61150N, 110.19640E, WGS 84), a protected area of 2,230 ha, located within the Matang Massif, the second from forests attached to a privately-owned farmland (1.30730N, 110.50370E, WGS 84), around the township of Serian (Image 1). Vegetation types represented include mixed dipterocarp forest, Kerangas (Bornean heath forest) and submontane forests (Hazebroek & Morshidi 2000). Data were obtained between 11 April 2017 and 30 January 2019 from five females that were fitted with temperature sensitive transmitters (HolohilTM Ri2B and HolohilTM PD-2T) for a study of spatial and thermal ecology, during which the present study was conducted. Animals were brought to a veterinary clinic for radiography and released at the point of encounter within a week.

Radiography procedures were conducted by a qualified veterinarian. A Sedecal Apr-Vet (Model E7239X) radiographic unit was used to produce three views per individual (dorsal, ventral and lateral positions). Each exposure was 78 kV (25 mA to 320 mA) for 0.08 sec, following which individuals were weighed using a digital scale (Camry/ ACS-3—JC31). General anaesthesia was not used in the procedure, and depending on the mobility of the individual turtle, manual restraints with tape was used. An Xscan Radiology Application (Version 2.10) was used to edit the image obtained, prior to examination.

                 

 

OBSERVATIONS AND DISCUSSION

 

A total of 34 radiographic images were taken of five females, which displayed a distinct sulcus, presumably comprising connective tissue, across the midbody, specifically transversely between the hyoplastral-hypoplastral bones, and the hypoplastral & xiphiplastral bones, under the abdominal and femoral scute regions. None of the 18 radiographs of the two males showed evidence of a sulcus (refer to Image 5), which has been referred in the literature as indicative of a plastral hinge (Mertens 1942, 1971; Bramble 1974; Waagen 1984). The feature is known to exist only in adult females of the species (Moll 1985), presumably to facilitate oviposition and perhaps to allow the passage of large eggs (Yasukawa et al. 2001; Joyce et al. 2012). Other sexually dimorphic features have been listed in Baizurah & Das (2021). Images 2–4 indicate that kinesis of plastral elements may be shown by H. spinosa as seen in two females (SNB 638 and SNB 641) across time. The smallest female (mean SCL of 125.1 mm) was beginning to display presence of such a gap (Image 3) indicating possible size at maturity of females in H. spinosa. Examination of the radiographs of these individuals do not indicate a greater development of the hinge at any particular month, as might be expected if the hinge becomes functional only periodically, for the passage of the eggs.

Previous studies have discussed that pelvic aperture dimensions may be a limiting factor in reproductive output, and how it relates to sexual dimorphism in some turtles (Clark et al. 2001; Matysiak et al. 2017; Cordero et al. 2018). Apart from pelvic size variation and reduced relative plastral length in males in increasing reproduction output, plastral kinesis can serve a similar function in increasing reproduction output. Plastral kinesis is thought to reduce pelvic strain in females during egg-laying (Legler 1960; Yasukawa et al. 2001). The first record of a plastral hinge in H. spinosa was by Mertens (1942, 1971), followed by the detailed examination of two females by Waagen (1984), who speculated that the structure is rather weak in adult females. Hence the likelihood that kinesis serves a probably protective mechanism is unlikely. It is important to note that these descriptions are not supported by histological data hence lacking the information needed to functionally validate female-specific plastral kinesis in Heosemys. Waagen (1984) described the hinge as consisting of fibrous tissues internally that did not appear to change with body size, although the possibility of temporal change was mentioned. As described in that study, the present one found that the structure does not remain distinct year round, the deossification of bones presumed related to oviposition, not affected by seasonal changes, as evidenced in our radiographs (see Images 1–3). However, we have no indication that any of our females were preparing to reproduce, and no mating behaviour was observed. Previous literature on reproduction of H. spinosa, albeit in captivity, stated that copulation is typically triggered by rain showers, and egg deposition usually occurs in March-July (Herman 1993; Goetz 2007). In Sarawak (northwestern Borneo), high humidity and temperatures are encountered throughout the year, and periods associated with high rainfall events occur between November and March, with the passage of the north-east monsoons, and a weaker one between May and September, coinciding with the south-west monsoons (Sa’adi et al. 2019).

Numerous functional traits usually emerge late in turtle ontogeny, including development of fibrous tissues, which are known to progress slowly via repatterning of tissue which is acquired over the growth period (Cordero et al. 2018). The gradual process may explain the changes in hyo-hypoplastral, and hypo-xiphiplastral regions we noted across time. For instance, hatchling plastron shape of kinetic-shelled species undergoes differentiation post embryonic stages, especially in area where the hinge presumably occurs, as they reached maturity, in contrast to akinetic species which undergoes plastron differentiation at extreme and posterior ends (Cordero et al. 2019). Lastly, extrinsic factors such as abundance of resources and rainfall are known to affect reproductive cycles in some species (Akani et al. 2005; Loehr et al. 2011; Graham et al. 2015). Our radiographic observations suggest that hyo-hypoplastral and hypo-xiphiplastral kinesis in H. spinosa is possibly influenced by reproductive needs, developing during ontogeny, and may not be associated with local climate.

 

 

Table 1. Details of Heosemys spinosa radiographically examined.

Identification

Sex

Total radiographs

Locality

SNB 637

Male

16

Kubah NP

SNB 638

Female

14

Kubah NP

SNB 639

Male

2

Kubah NP

SNB 641

Female

12

Kubah NP

SNB 642

Female

2

Kubah NP

SNB 643

Female

4

Kubah NP

SNB 640

Female

2

Serian

 

 

For images - - click here for full PDF

 

 

REFERENCES

 

Angielczyk, K.D. (2011). Adaptive evolution of plastron shape in emydine turtles. Evolution 65(2): 377–394. https://doi.org/10.1111/j.1558-5646.2010.01118.x

Akani, G.C., M. Francesco, M. Angelici, S. Wariboko, E. Politano, E. Filippi & L. Luiselli (2005). Reproductive seasonality and clutch size of sympatric Hinge-back Tortoises (Kinixys erosa and Kinixys homeana) in southern Nigeria (Reptilia, Testudines: Testudinae). Aldrovandia 1: 111–115.

Baizurah, S.N. & I. Das (2021). Sexual dimorphism in Heosemys spinosa (Testudines: Geoemydidae) from Sarawak, Borneo. Herpetology Notes 14: 1231–1235. https://www.biotaxa.org/hn/article/view/67247

Berlant, Z.S. & C.T. Stayton. (2017). Shell morphology in the Kinosternidae: functional and evolutionary patterns. Herpetologica 73(1): 30–42. https://www.jstor.org/stable/26534350

Bramble, D.M. (1974). Emydid shell kinesis: biomechanics and evolution. Copeia 1974(3): 707–727. https://www.jstor.org/stable/1442685?origin=crossref

Clark, P.J., M.A. Ewert & C.E. Nelson (2001). Physical apertures as constraints on egg size and shape in the Common Musk Turtle, Sternotherus odoratus. Functional Ecology 15(1): 70–77. https://doi.org/10.1046/j.1365-2435.2001.00494.x

Cordero, G.A. & K. Quinteros (2015). Skeletal remodelling suggests the turtle’s shell is not an evolutionary straitjacket. Biology Letters 11(4): 1–5. https://doi.org/10.1098/rsbl.2015.0022

Cordero, G.A., K. Quinteros & F.J. Janzen (2018). Delayed trait development and the convergent evolution of shell kinesis in turtles. Proceedings of the Royal Society B 285(1888): 20181585. https://doi.org/10.1098/rspb.2018.1585

Cordero, G.A., S. Stearns, K. Quinteros, C.M. Berns, S.M. Binz & F.J. Janzen (2019). The postembryonic transformation of the shell in emydine box turtles. Evolution and Development 21: 297–310. https://doi.org/10.1111/ede.12307

Ernst, C.H. & R.W. Barbour (1989). Turtles of the World. Smithsonian Institution Press, Washington, D.C., 313 pp.

Goetz, M. (2007). Husbandry and breeding of the Spiny Turtle Heosemys spinosa (Gray, 1831) at the Durrell Wildlife Conservation Trust. Radiata 16(2): 1–15.

Graham, S.P., C.K. Ward, J.S. Walker, S. Sterrett & M.T. Mendonca (2015). Sexual dimorphism and seasonal variation of reproductive hormones in the Pascagoula Map Turtle, Graptemys gibbonsi. Copeia 2015(1): 42–50.

Hazebroek, H.P. & A.K.A. Morshidi (2000). National Park of Sarawak. Natural History Publication (Borneo) Sdn Bhd., Kota Kinabalu.

Herman, D.W. (1993). Reproduction and management of the southeast Asian Spiny Turtle (Heosemys spinosa) in captivity. Herpetological Natural History 1(1): 97–100.

Hofmeyr, M.D., B.T. Henen & V.J.T. Loehr (2005). Overcoming environmental and morphological constraints: egg size and pelvic kinesis in the smallest tortoise, Homopus signatus. Canadian Journal of Zoology 83: 1343–1352. https://cdnsciencepub.com/doi/10.1139/z05-132

Joyce, W.G., N. Micklich, S.F.K. Schaal & T.M. Scheyer. (2012). Caught in the act: The first record of copulating fossil vertebrates. Biology Letters 8: 846–848. https://royalsocietypublishing.org/doi/10.1098/rsbl.2012.0361

Legler, J.M. (1960). Natural history of the Ornate Box Turtle, Terrapene ornata ornata Agassiz. University of Kansas Publications, Museum of Natural History 11: 527–669.

Loehr, V.J.T., B.T. Henen & M.D. Hofmeyr (2011). Reproductive responses to rainfall in the Namaqualand Speckled Tortoise. Copeia 2011(2): 278–284. https://www.jstor.org/stable/41261877

Matysiak, A., A.W. Malecha, H. Jakubowski, E.T. Sadowska, P. Koteja & P. Tryjanowski (2017). Sexual dimorphism, asymmetry and the effect of reproduction on pelvis bone in the bank vole, Myodes glareolus. Mammal Research 62(3): 297–306. https://doi.org/10.1007/s13364-017-0317-1

Mertens, R. (1942). Zwei bemerkungen über Schildkröten Südost-Asiens. Senckenbergiana 25(1/3): 41–46.

Mertens, R. (1971). Die Stachelschildkröte (Heosemys spinosa) and ihre Verwandten. Salamandra 7(2): 49–54.

Moll, E.O. (1985). Comment: sexually dimorphic plastral kinesis– the forgotten papers. Herpetological Review 16: 16.

Pritchard, P.C.H. (1993). Carapacial pankinesis in the Malayan Softshell Turtle, Dogania subplana. Chelonian Conservation and Biology 1(1): 31–36. https://chelonian.org/wp-content/uploads/file/CCB%20Vol%201%20No%201%20(1993)/Pritchard_1993a.pdf

Pritchard, P.C.H. (2003). Akinesis and plastral scute homologies in Sternotherus (Testudines: Kinosternidae). Chelonian Conservation and Biology 4(3): 671–674. https://chelonian.org/wp-content/uploads/file/CCB_Vol_4_Nos1-4(2001-2005)/Pritchard_2003.pdf

Pritchard, P.C.H. (2008). Evolution and structure of the turtle shell, pp. 45–84. In: Wyneken, J., M.H. Godfrey & V. Bels (eds.). Biology of Turtles: From Structures to Strategies of Life. CRC Press, Boca Raton, Florida, USA.

Rivera, G. (2008). Ecomorphological variation in shell shape of the freshwater turtle Pseudemys concinna inhabiting different aquatic flow regimes. Integrative and Comparative Biology 48(6): 769–787. https://doi.org/10.1093/icb/icn088

Sa’adi, Z., S. Shahid, T. Ismail, E.-S. Chung & X.-J. Wang (2019). Trends analysis of rainfall and rainfall extremes in Sarawak, Malaysia using modified Mann–Kendall test. Meteorology and Atmospheric Physics 131: 263–277. https://doi.org/10.1007/s00703-017-0564-3

Waagen, G.N. (1984). Sexually dimorphic plastral kinesis in Heosemys spinosa. Herpetological Review 15(2): 33–34.

Williams, C. & C.T. Stayton (2019). Effects of sutured pelvic elements: a comparison of pleurodire and cryptodire shell mechanics. Herpetologica 75(2): 123–133. https://doi.org/10.1655/D-17-00066

Yasukawa, Y., R. Hirayama & T. Hikida (2001). Phylogenetic relationships of Geoemydine turtles (Reptilia: Bataguridae). Current Herpetology 20(2): 105–133. https://www.jstage.jst.go.jp/article/hsj2000/20/2/20_2_105/_pdf/-char/en