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Reptile Ecology and Conservation

Techniques in Ecology and Conservation Series

Series Editor: William J. Sutherland

Bird Ecology and Conservation: A Handbook of Techniques

William J. Sutherland, Ian Newton, and Rhys E. Green

Conservation Education and Outreach Techniques

Susan K. Jacobson, Mallory D. McDuff, and Martha C. Monroe

Forest Ecology and Conservation: A Handbook of Techniques

Adrian C. Newton

Habitat Management for Conservation: A Handbook of Techniques

Malcolm Ausden

Conservation and Sustainable Use: A Handbook of Techniques

E.J. Milner-Gulland and J. Marcus Rowcliffe

Invasive Species Management: A Handbook of Principles and Techniques

Mick N. Clout and Peter A. Williams

Amphibian Ecology and Conservation: A Handbook of Techniques

C. Kenneth Dodd, Jr.

Insect Conservation: A Handbook of Approaches and Methods

Michael J. Samways, Melodie A. McGeoch, and Tim R. New

Remote Sensing for Ecology and Conservation: A Handbook of Techniques

Ned Horning, Julie A. Robinson, Eleanor J. Sterling, Woody Turner, and Sacha Spector

Marine Mammal Ecology and Conservation: A Handbook of Techniques

Ian L. Boyd, W. Don Bowen, and Sara J. Iverson

Carnivore Ecology and Conservation: A Handbook of Techniques

Luigi Boitani and Roger A. Powell

Primate Ecology and Conservation: A Handbook of Techniques

Eleanor J. Sterling, Nora Bynum, and Mary E. Blair

Conservation Education and Outreach Techniques Second Edition

Susan K. Jacobson, Mallory D. McDuff, and Martha C. Monroe

Reptile Ecology and Conservation: A Handbook of Techniques

C. Kenneth Dodd, Jr.

Reptile Ecology and Conservation

A Handbook of Techniques

Edited by C. Kenneth Dodd, Jr.

3

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In memory of Jonathan Scott Loftis

Preface

As this volume is completed, more than 10,200 non-avian reptile species have been rec- ognized (6175 lizards and amphisbaenians, 3496 snakes, 341 turtles, 25 crocodilians, and 1 Tuatara), with new taxa being described nearly every day (Uetz, P. and Hošek, J. (eds), The Reptile Database, http://www.reptile-database.org, accessed 17 August 2015). The life histories and conservation status of most of these species are imper- fectly understood or completely unknown except for a few of the more charismatic or popular larger species. Because of a host of threats such as habitat loss and fragmenta- tion, trade, toxic and endocrine disrupting chemicals, emerging infectious diseases, and global climate change, it seems likely that reptiles may be declining at rates approaching those of amphibians (Gibbons et al., 2000; Böhm et al., 2013) and that many spe- cies will disappear by the end of the twenty-first century (Alroy, 2015; Ceballos et al., 2015; McCallum, 2015). At the same time, powerful economic interests have united to adversely influence decisions affecting the environment, even rejecting well-established scientific research such as the origin and extent of climate change. There is thus an urgent need for field research on reptile species and their community interactions. There are a great many techniques available for ecological and conservation-based research on reptiles. Journals such as Herpetological Review, Herpetological Conservation and Biology, and Chelonian Conservation and Biology frequently contain techniques papers. Specialized books and papers, such Henle and Veith (1997), Gent and Gibson (1998), Hachtel et al. (2009), Eekhout (2010), McDiarmid et al. (2012), Cacciali (2013), and Graeter et al. (2013), offer additional summaries that are as applicable today as when they were published. Although not strictly a techniques book, many of the chapters in Lutterschmidt (2013) offer excellent guides as to the dynamic state of research in reptile biology currently underway. The current volume is meant not to supplant earlier works, but to supplement them and add new areas not previously sum- marized, such as statistical modelling, landscape ecology, genetics, disease-biosecurity, and human dimensions. Our objectives have been to delineate important new develop- ments, to give an idea as to what the techniques tell or do not tell a researcher, to focus attention on biases and data inference, and to get readers to appreciate sampling as an integral part of their science, rather than just a means of capturing animals. The tech- niques used will set the boundaries within which results can or should be interpreted. No one volume can include all techniques, nor can the techniques included be dis- cussed in more than passing detail. Because of space limitations, chapters on growth (Andrews, 1982), behaviour, advanced spatial modelling, social science, relocation/ reintroduction (see Animal Conservation, Volume 17, Supplement 1, 2015), and the use of stable isotopes (Fry, 2006) could not be included. Authors of individual chapters were advised to incorporate some of these topics as best they could into existing chapters, and to point readers to important references where more detailed information may be obtained. In addition, many of the topics covered in the amphibian volume of this series

viii | Preface

also are pertinent to reptiles (Dodd, 2010). Lack of space also precludes the addition of a comprehensive glossary. Readers should consult Lillywhite (2008) or online sources when unfamiliar terms are encountered. Publishing results is an integral component of research undertaken on reptile ecology and conservation. It is simply not good enough to bury research findings in unpublished reports or university theses. Although not all investigations result in ‘high impact’ pub- lications, there are myriad outlets available for disseminating research results. At the same time, researchers should avoid so-called ‘predatory’ or ‘pay to publish’ journals, as publication in journals of dubious scholarly reputation will lead to a questioning of research reliability and interpretation. A list of questionable publishers can be found at:

http://scholarlyoa.com/publishers/. The editor thanks the following for taking their valuable time assisting with vari- ous aspects of this project: Matthew Allender, George Balazs, Jaime Bertoluci, Bayard Brattstrom, Steven J.B. Carter, Michael Cherkiss, William Cooper, Ben Croak, Wei- Guo Du, Ruth Elsey, Kevin Enge, Neil Ford, Mercedes Foster, Frank Glaw, Gurutzeta Guillera-Arroita, April Goodman Hall, John Iverson, Kate Jackson, Ambika Kamath, Joshua Kapfer, Amy Lathrop, Harvey Lillywhite, Peter Lindeman, Scott Loarie, Victor Loehr, Erin Marnocha, Jonathan Mawdsley, Shai Meiri, Damian Michael, Donald B. Miles, Debra Miller, Joe Mitchell, Akira Mori, Paul Ouboter, Ted Papenfuss, Michael Plummer, Thomas Rainwater, John H. Roe, Jose Rosado, Christopher Rowe, Andrew Royle, Raul F.D. Sales, Benedikt Schmidt, Coleman Sheehy, Rick Shine, Cameron Siler, Javier Manjarrez Silva, Lora Smith, Phillip Q. Spinks, James Spotila, Laurie Vitt, Jayme Waldron, Dan Warner, James Watling, Kimberley M. Watson, Grahame Webb, Scott Weir, Allan Woodward, and Amy Yackel. I greatly appreciate the support from Ian Sherman and Lucy Nash at Oxford University Press, and thank series editor, Bill Sutherland, for inviting me to edit the reptile volume. Alan Skull and Indumadhi Srinivasan deserve special thanks for their efforts to improve the text and illustrations. A special thanks to Marian Griffey, Morganna Fairchild (feline, not the actress), Allen K. Fearless, and the rest of the cat pride. This volume is dedicated to all the biologists who take up the challenge of reptile ecology and conservation.

C. Kenneth Dodd, Jr.

References

Alroy, J. (2015). Current extinction rates of reptiles and amphibians. Proceedings of the National Academy of Science, USA, DOI: 10.1073/pnas.1508681112. Andrews, R.M. (1982). Patterns of growth in reptiles. In C. Gans (ed) Biology of the Reptilia, Volume 13. Physiology D: Physiological Ecology. London: Academic Press, pp. 273–320. Böhm, M., Collen, B., Baillie, J.E.M., et al. (2013). The conservation status of the world’s rep- tiles. Biological Conservation, 157, 372–85. Cacciali, P. (2013). Colecta y Preparación de Anfibios y Reptiles. Saarbrücken, Germany: Editorial Académica Española, AV Akademikerverlag GmbH & Co. Ceballos, G., Ehrlich, P.R., Barnosky, A.D., et al. (2015). Accelerated modern human-induced species losses: entering the sixth mass extinction. Science Advances, 1, e1400253. Dodd, C.K., Jr. (ed). (2010). Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford: Oxford University Press.

Preface |

ix

Eekhout, X. (2010). Sampling amphibians and reptiles. ABC Taxa, 8, 530–57. Fry, B. (2006). Stable Isotope Ecology. New York: Springer Science. Gent, T., and Gibson, S. (eds). (1998). Herpetofauna Worker’s Manual. Peterborough, UK: Joint Nature Conservation Committee. Gibbons, J.W., Scott, D.E., Ryan, T.J., et al. (2000). The global decline of reptiles, déjà vu amphibians. Bioscience, 50, 653–66. Graeter, G.K., Buhlmann, K.A., Wilkinson, L.R., et al. (eds). (2013). Inventory and Monitoring:

Recommended Techniques for Amphibians and Reptiles. Technical Publication IM-1. Birmingham, AL: Partners in Amphibian and Reptile Conservation. Hachtel, M., Schlüpmann, M, Thiesmeier, B., et al. (eds). (2009). Methoden der Feldherpetologie. Bielefeld, Germany: Laurenti Verlag. Henle, K., and Veith, M. (eds). (1997). Naturschutzrelevante Methoden der Feldherpetologie. Deutsche Gesellschaft für Herpetologie und Terrarienkunde. Lillywhite, H.B. (2008). Dictionary of Herpetology. Malabar, FL: Krieger Publishing. Lutterschmidt, W.I. (ed). (2013). Reptiles in Research. Investigations of Ecology, Physiology, and Behavior from Desert to Sea. New York: Nova Biomedical. McCallum, M.L. (2015). Vertebrate biodiversity losses point to a sixth mass extinction. Biodiversity and Conservation, DOI: 10.1007/s10531-0940-6. McDiarmid, R.W., Foster, M.S., Guyer, C., et al. (eds). (2012). Reptile Biodiversity. Standard Methods for Inventory and Monitoring. Berkeley, CA: University of California Press.

Contents

List of Contributors

Part 1. Introduction

xxv

1.

Reptile diversity and life history

3

Laurie J. Vitt

 
 

1.1 Introduction

3

1.2 Reptile ‘diversity’

3

 

1.2.1 ‘Diversity’

3

1.2.2 Evolutionary history and numbers of reptile species

3

1.2.3 Morphological and ecological diversity

5

 

1.3

Diversity of life histories

8

 

1.3.1 Definitions

8

1.3.2 General observations

8

1.3.3 Turtle life histories

8

1.3.4 Crocodilian life histories

8

1.3.5 Squamate life histories

10

1.3.6 Tuatara life history

11

 

1.4

Summary

12

 

References

13

2. Planning and setting objectives in field studies

Robert N. Fisher

16

2.1 Introduction

16

2.2 Planning: goals versus objectives

16

2.3 Design

17

2.4 Conceptual models

19

2.5 Sampling considerations

20

2.6 Covariates

24

2.7 Timescales

24

2.8 Permits

25

2.9 Ethical considerations

28

2.10 Biosecurity

29

2.11 Conclusion

30

2.12 Example URLs for SMART objectives

30

xii | Contents

3. Data collection and storage

Richard A. Seigel

32

3.1 Introduction

32

3.2 Flexibility: the research proposal versus the real world

33

3.3 Field notes

34

 

3.3.1 Mechanics of field notes

34

3.3.2 The field notebook

35

3.3.3 What to record and how to record it

36

3.4

Data sheets

38

3.4.1 General considerations

38

3.4.2 Mechanics of data sheets

38

3.5 Documenting the field site: photographs, GIS, and environmental data

39

3.6 Data: backing up and archiving

40

 

3.6.1 Data backups

41

3.6.2 Data archiving and metadata

41

3.7

Conclusions

42

Acknowledgements

42

 

References

42

Part 2. The Individual

4. Marking and measuring reptiles

John W. Ferner and Michael V. Plummer

45

4.1 Introduction

45

4.2 Toe-clipping

46

4.3 Scale/scute-clipping

47

4.3.1 Snakes

47

4.3.2 Lizards

48

4.4 Branding and painting

49

4.4.1 Turtles

49

4.4.2 Lizards

50

4.4.3 Snakes

50

4.5 Shell notching

51

4.6 Tagging and banding

52

4.6.1 Lizards

52

4.6.2 Freshwater and terrestrial turtles

53

4.6.3 Snakes

54

4.7 Trailing devices

54

4.8 Passive integrated transponder (PIT) tags

54

4.8.1 Turtles

55

4.8.2 Lizards and snakes

55

Contents | xiii

5.

4.10 Recommendations

56

References

56

Digital identification and analysis

59

Roberto Sacchi, Stefano Scali, Marco Mangiacotti, Marco Sannolo, and Marco A.L. Zuffi

5.1 Introduction

 

59

5.2 Collecting images

61

 

5.2.1 Identification of distinctive features

62

5.2.2 Set-up of a photographic shoot

62

5.2.3 Photo shooting

63

5.2.4 Photo coding

63

5.2.5 Photo enhancement

63

5.3

Software and algorithms

63

5.3.1 I 3 S, Interactive Individual Identification System

63

5.3.2 Wild-ID

64

5.3.3 MYDAS

64

5.3.4 APHIS

65

5.4 How they work

65

5.5 Validation

 

66

5.6 Photo-identification in reptiles: present and future

69

 

5.6.1

The state of the art of photo-identification in reptiles

69

5.6.2

Where should we go from here?

71

References

71

6. Preserving reptiles for research

Steve W. Gotte, Jeremy F. Jacobs, and George R. Zug

73

6.1 Introduction

73

6.2 Planning and permits

74

6.3 Euthanasia

75

6.4 Specimen preservation and data collection

77

6.4.1 Record keeping

77

6.4.2 Preservation and positioning

79

6.5 Specimen transport and shipping

84

6.6 Useful resources

84

Acknowledgements and notice

85

References

85

7. Reproduction

87

Gunther Köhler

7.1 Introduction

87

xiv | Contents

7.3

Dissections

89

7.4 Endoscopy

91

7.5 External examination and palpation

92

7.6 Imaging methods

93

7.7 Blood chemistry

93

7.8 Hormonal induction of egg laying

94

7.9 Conclusions

94

 

References

94

8. Diet

97

Luca Luiselli and Giovanni Amori

8.1 Introduction

97

8.2 Sources of material

97

8.3 Methods for examining diet and trophic interactions

99

8.3.1 Direct observation

99

8.3.2 Dissection of stomachs

99

8.3.3 Stomach flushing

100

8.3.4 Faecal pellets

102

8.3.5 Forced regurgitation

103

8.3.6 Stable isotopes

104

8.3.7 Doubly labelled water

104

8.4 Diet by volume or mass vs. diet by prey number

105

8.5 Gut clearance times

105

8.6 Quantitative analyses of diet

106

References

107

9. Movement patterns and telemetry

Bruce A. Kingsbury and Nathan J. Robinson

110

9.1 Introduction

110

9.2 Common considerations for telemetry studies

110

9.3 Telemetry devices

111

9.3.1 VHF transmitters

111

9.3.2 Acoustic telemetry

113

9.3.3 Satellite telemetry

113

9.4 Statistical techniques for analysing telemetry data

114

9.5 Taxonomic considerations

116

9.5.1 Terrestrial and freshwater turtles

116

9.5.2 Lizards and snakes

117

9.5.3 Crocodilians

118

9.5.4 Sea turtles

118

9.6 Future directions

119

Contents | xv

Part 3. Sampling Reptiles

10. Surface-dwelling reptiles

John D. Willson

125

10.1 Introduction

125

10.2 Selecting a capture method

125

10.2.1 Study goals and preliminary considerations

126

10.2.2 Capture rates

127

10.2.3 Cost and effort

127

10.2.4 Repeatability

127

10.2.5 Bias

128

10.3 Active capture techniques

128

10.3.1 Visual encounter surveys

128

10.3.2 Cover boards

129

10.3.3 Road surveys

130

10.3.4 Lizard noosing

131

10.3.5 Considerations and limitations

131

10.4 Passive capture techniques

131

10.4.1 Pitfall traps

131

10.4.2 Funnel traps

132

10.4.3 Drift fences

134

10.4.4 Considerations and limitations

134

10.5 Conclusions and recommendations

136

References

136

11. Arboreal and fossorial reptiles

Robert W. Henderson, Robert Powell, Jose Martín, and Pilar Lopez

139

11.1 Arboreal reptiles

139

11.1.1 Introduction

139

11.1.2 General methods

140

11.1.3 Collecting methods

140

11.2 Fossorial reptiles

146

11.2.1 Introduction

146

11.2.2 Active searching

146

11.2.3 Below-ground trapping

149

References

150

12.

Sea snakes

154

Xavier Bonnet, Arne R. Rasmussen, and François Brischoux

12.1 Introduction

154

12.2 Locating, catching, and identifying sea snakes

155

12.2.1 Locating and catching snakes

155

12.2.2 Amphibious sea snakes on land

155

xvi | Contents

12.3 Identifying sea snakes

157

12.4 Measuring and describing sea snakes

158

12.5 Photographing sea snakes

159

12.6 Recapture studies

160

12.6.1 Marking snakes

160

12.6.2 Organizing data

161

12.7 Blood and other tissue sampling

161

12.8 Bio-logging

162

12.9 Captivity

163

12.10 Conclusions

163

References

165

13. Freshwater turtles

Richard C. Vogt

168

13.1 Aquatic turtles on land

168

13.1.1 Miscellaneous techniques

168

13.1.2 Nest surveys

169

13.2 Aquatic turtles in water

169

13.2.1 Surprise, snorkelling, muddling, and polling

169

13.2.2 Basking traps

171

13.2.3 Basking surveys

171

13.2.4 Trapping

172

13.3 Capture biases

178

Acknowledgements

178

References

178

14. Terrestrial turtles and tortoises

Margaretha D. Hofmeyr and Brian T. Henen

181

14.1 Introduction

181

14.2 Concepts in survey design

181

14.3 Review of survey methods

184

14.3.1 Mark–recapture

184

14.3.2 Visual encounter surveys

185

14.3.3 Line distance sampling

187

14.3.4 Surrogates

188

14.3.5 Wildlife detector dog surveys

189

14.3.6 Other methods

190

14.4 Conclusions

191

Contents | xvii

15.

Sea turtles

Seth Stapleton and Karen L. Eckert

194

15.1 Introduction

194

15.2 Monitoring nesting beaches

196

15.2.1

Ground-based methods

196

15.2.2

Aerial survey methods

198

15.2.3

Nesting crawl identifications

199

15.2.4

Locating nests

200

15.2.5

Egg counts and nest excavations

202

15.3 Tagging

203

15.4 Local interviews

205

15.5 Summary

206

References

207

16. Crocodilians

Matthew Brien and Charlie Manolis

211

16.1 Introduction

211

16.2 Surveying

211

16.2.1

Spotlight surveys

211

16.2.2

Aerial count surveys

214

16.2.3

Day count surveys

214

16.2.4

Nest counts

214

16.2.5

Other survey methods

215

16.3 Capture

215

16.3.1

Hand capture or tongs

215

16.3.2

Noosing

215

16.3.3

Skin harpoon

216

16.3.4

Traps

216

16.3.5

Snatch hook

217

16.3.6

Fixed-position snares

217

16.3.7

Nets

217

16.3.8

Baited hooks

218

16.3.9

Baited digestible ‘hooks’

218

16.4 Handling

218

16.4.1

Controlling the head

218

16.4.2

Securing the jaws

219

16.4.3

Restraining the limbs

219

16.4.4

Temporary holding and transport

219

16.4.5

Immobilizing agents

219

16.5 Tagging

220

xviii | Contents

16.5.2

Webbing tags

221

16.5.3 PIT tags

221

16.5.4 Ear tags

221

16.5.5

Anchor fish tags

221

16.5.6

Electronic tags

221

References

222

Part 4. Reptiles in the Community

17. Plot and transect censuses

Tiffany M. Doan

227

17.1 Introduction

227

17.2 Trade-off between intensity and area

228

17.3 Plots versus transects

229

17.4 Valid implementation of plot and transect techniques

230

17.5 Standard plot and transect techniques

232

17.5.1

Visual encounter surveys on trails

232

17.5.2

Line transects

233

17.5.3 Quadrats

233

17.5.4 Total removal plots

234

17.5.5 Other plot and transect techniques

235

17.6 Individual and habitat variables

236

17.7 Selecting the appropriate plot and transect techniques

236

Acknowledgements

238

References

238

18. Rapid assessments of reptile diversity

Indraneil Das

241

18.1 Introduction

241

18.2 What is an RA?

242

18.3 Planning components of RAs

242

18.3.1

Assembling literature and other resources

242

18.3.2

Permitting

243

18.3.3

Training of field personnel

243

18.3.4

Timing

244

18.4 Field sampling

244

18.4.1 Community questionnaire surveys

244

18.4.2 Visual encounter survey

245

18.4.3 Species list technique

246

18.4.4 Trapping

246

18.4.5 Taxon-specific techniques

246

18.4.6 Environmental DNA

248

Contents | xix

18.6

Summary

249

Acknowledgements

250

References

250

19. Measuring microhabitats used by non-avian reptiles

Henry R. Mushinsky and Earl D. McCoy

254

20.

19.1 Introduction

254

19.2 Types of habitats and variables

257

19.3 Marine habitats: sea and brackish water turtles, sea snakes, crocodiles, marine iguanas

260

19.4 Freshwater habitats: freshwater turtles, water snakes, alligators, caimans

261

19.5 Terrestrial habitats: most lizards, most snakes, terrestrial turtles, Tuatara

263

19.6 Rocky habitats: lizards and snakes

264

19.7 Fossorial habitats: some lizards, amphisbaenids, some snakes

265

19.8 Arboreal habitats: some snakes, some lizards

266

19.9 Summary and recommendations

267

Acknowledgements

268

References

268

Water quality and toxicology

272

Christine Bishop

20.1 Introduction

272

20.2 Measurement of exposure and interpreting concentrations

273

20.3 Field collections to measure contamination in air, water, sediment, biota

273

20.3.1 Water, sediment, and biota sample container preparation for trace analyses

274

20.3.2 Sediments

274

20.3.3 Water

274

20.3.4 Water and sediment chemistry

275

20.3.5 Passive integrative samplers for air and water

275

20.4 Measurement of levels and effects of environmental contamination in reptiles

275

20.4.1 Measurement of contaminants in reptiles

275

20.4.2 Eggs

276

20.4.3 Internal organs and bone

276

20.4.4 Blood and plasma

276

20.4.5 Scales, claws, tails, scutes

277

20.5 Measurement of effects of environmental contaminants on reptiles

277

20.6 Population level effects of environmental contaminants in reptiles

279

20.7 Summary

279

xx | Contents

21. Richness, diversity, and similarity

C. Kenneth Dodd, Jr.

283

21.1 Introduction

283

21.2 Data transformation

283

21.3 Species diversity

285

21.3.1 Sampling considerations

285

21.3.2 Species richness

286

21.3.3 Species accumulation curves

287

21.3.4 Heterogeneity

288

21.3.5 Evenness and dominance

290

21.4 Similarity

290

21.5 Software

293

21.6 Summary

294

References

294

22. Landscape ecology, biogeography, and GIS methods

Monika Böhm and Viorel D. Popescu

298

22.1 Introduction

298

22.1.1 Landscape ecology, biogeography, and macroecology

298

22.1.2 Geographic information systems (GIS)

299

22.2 Landscape ecology concepts applied to reptile ecology and conservation

303

22.2.1 Landscape composition and configuration

303

22.2.2 Structural and functional connectivity

303

22.2.3 Landscape thresholds and conservation management decision-making

305

22.2.4 Edge effects

306

22.3 GIS for species conservation

306

22.3.1 Modelling and mapping species distributions

306

22.3.2 Landscape ecology for reptile conservation

307

22.3.3 Macroecology and biogeography for reptile conservation

308

22.4 Spatial statistics: the analysis of spatially correlated data

310

22.5 Shortcomings and future directions

311

References

313

Part 5. Experimental Applications, Physiological Ecology, and Genetics

23. Experimental applications

Stephen J. Mullin

317

23.1 Introduction

317

23.2 Selecting species

318

Contents | xxi

 

23.2.2 Aquatic and semi-aquatic species

318

23.2.3 Additional considerations

319

23.3

Studies using cages

320

23.3.1 Lab-based mesocosms

320

23.3.2 In situ habitat enclosures

321

23.3.3 Cage construction and siting

326

23.3.4 The utility of zoological parks

328

23.4

Manipulative applications

328

23.4.1 Manipulating habitat

329

23.4.2 Manipulating individuals

329

23.5

Conclusions

331

Acknowledgements

332

References

332

24. Body temperatures and the thermal environment

Keith A. Christian, Christopher R. Tracy, and C. Richard Tracy

337

24.1 Introduction

337

24.1.1 The importance thermal biology

337

24.1.2 The importance of using appropriate techniques to study thermal biology

337

24.1.3 Historical perspective

338

24.2 Techniques for quantifying thermal biology

342

24.2.1 Computational models

342

24.2.2 Physical models

343

24.3 Advantages and disadvantages of computational and physical models

344

24.4 Use of data loggers as surrogate physical T e models

345

24.5 Thermal transients

345

24.5.1 How to account for thermal transients in large animals

346

24.5.2 How big does an animal have to be before it is ‘large’?

347

24.6 Conclusions

347

References

349

25. Genetics in field ecology and conservation

Nancy N. FitzSimmons and Joanna Sumner

352

25.1 Introduction

352

25.2 Genetic markers

353

25.2.1 Allozymes and restriction fragment length polymorphisms

353

25.2.2 Mitochondrial DNA sequencing

354

25.2.3 Nuclear gene sequencing

355

25.2.4 Nuclear microsatellites

356

25.2.5 Single nucleotide polymorphisms

357

xxii | Contents

25.3 Initiating a genetic study

358

25.4 Labwork

359

25.5 Sample design

359

25.6 Sample collection and storage

360

25.6.1 Sampling considerations

360

25.6.2 Sample preservation

361

25.6.3 Long-term storage

361

25.6.4 Sample curation

361

25.7 Data analysis and management

361

References

362

Part 6. Trends Analysis and Conservation Options

26. Occupancy models

Darryl I. MacKenzie

373

26.1 Introduction

373

26.2 Method overview

374

26.3 Grand Skink example

377

26.4 Recent extensions

380

26.4.1 Multi-state occupancy

381

26.4.2 Multi-scale occupancy

381

26.4.3 Species misidentification

382

26.4.4 Correlated detections

382

26.5 Response to criticisms

383

26.6 Summary

384

References

386

27. Estimating abundance

Chris Sutherland and J. Andrew Royle

388

27.1 Introduction

388

27.2 Closed population capture–recapture

388

27.2.1 Sampling a population

388

27.2.2 Estimating abundance using model M 0

390

27.2.3 Variation in p: beyond M 0

391

27.2.4 Removal sampling

391

27.2.5 Hierarchical capture–recapture models

392

27.2.6 Individual covariate models and distance sampling

392

27.2.7 Spatial capture–recapture

394

27.3 Software

395

27.4 Example: population size and density estimation of Slow Worms

396

27.5 Summary

398

Contents | xxiii

28. Collecting biological samples for disease monitoring

Elliott R. Jacobson

402

28.1 Introduction

402

28.2 Ethics and animal welfare

402

28.3 Institutional Animal Care and Use Committees

403

28.4 Pain

404

28.5 Analgesia and anaesthesia

404

28.5.1 Local analgesics and central acting injectable anaesthetics

404

28.5.2 Inhalant anaesthetics

405

28.5.3 Post-surgical analgesia

405

28.6 Major infectious and non-infectious diseases

405

28.6.1 Infectious diseases

405

28.6.2 Non-infectious diseases

408

28.7 Collecting samples for disease diagnostics

409

28.7.1 Equipment

409

28.7.2 Blood collection and handling

410

28.7.3 Serology

411

28.7.4 Biopsies

411

28.7.5 Pathological evaluations

412

28.7.6 Cytodiagnostics

412

28.7.7 Microbiology

412

28.7.8 Molecular diagnostics

413

28.7.9 Preserving ecto- and endoparasites for identification

414

28.8 Biosecurity: preventing pathogen transmission

414

28.9 Conclusions

415

References

415

29. Conservation management

David A. Pike

419

29.1 Introduction

419

29.1.1 Statutory protection

420

29.1.2 Habitat protection

421

29.1.3 Managing reptile populations

421

29.1.4 Monitoring populations

422

29.2 Habitats

422

29.2.1 Contiguous habitats, buffer zones, and edge effects

422

29.2.2 Habitat connectivity

426

29.2.3 Crossing transportation corridors

427

29.2.4 Microhabitats

428

29.3 Human-altered habitats

428

29.3.1

Agricultural landscapes

428

xxiv | Contents

29.3.3 Urban environments

430

29.3.4 Environmental contaminants

430

29.4 Intensive manipulation of individuals

430

29.4.1 Captive breeding

430

29.4.2 Relocation, repatriation, translocation (RRT)

431

29.4.3 Pest reduction

432

29.4.4 Biosecurity and disease

432

29.5 Conclusion

433

References

433

30. Education and outreach

Brian Gratwicke, Matthew Neff, Lindsay Renick Mayer, Sharon Ryan, and Jennifer Sevin

436

 

30.1 Introduction

436

30.2 Setting goals

437

30.3 Campaigns and constituency-building

437

30.3.1

Audience

438

30.3.2

Story

438

30.3.3 Constituency-building

439

30.3.4 Community conservation

440

30.4 Nature centres, museums, and exhibits

440

30.5 Citizen science

442

30.6 Engaging teachers and schools

444

30.7 Tips for designing educational programmes for schoolchildren

444

30.8 Leadership development

445

30.9 Summary

446

References

446

Index

449

List of Contributors

Giovanni Amori CNR-Institute of Ecosystem Studies, viale dell’Università 32, 00185 Rome, Italy. E-mail: giovanni.amori@uniroma1.it

Christine Bishop Environment Canada, Science and Technology Branch, Wildlife Research Division, 5421 Robertson Road, Delta, BC V4K 3N2, Canada. E-mail: cab.bishop@canada.ca

Monika Böhm Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK. E-mail: monika.bohm@ioz.ac.uk

Xavier Bonnet CEBC-CNRS, 79360 Villiers en Bois, France. E-mail: bonnet@cebc.cnrs.fr

Matthew Brien IUCN-SSC Crocodile Specialist Group, 6 Fitzmaurice Drive, Bentley Park, QLD 4869, Australia. E-mail: matthew_brien@hotmail.com

François Brischoux CEBC-CNRS, 79360 Villiers en Bois, France. E-mail: francois.brischoux@gmail.com

Keith A. Christian Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia. E-mail: keith.christian@cdu.edu.au

Indraneil Das Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia. E-mail: idas@ibec.unimas.my

Tiffany M. Doan Department of Biology, University of Central Florida, 4000 Central Florida Boulevard, Orlando, FL 32816, USA. E-mail: tiffperu@yahoo.com

C. Kenneth Dodd, Jr. Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611, USA. E-mail: Terrapene600@gmail.com

Karen L. Eckert Wider Caribbean Sea Turtle Conservation Network, 1348 Rusticview Drive, Ballwin, MO 63011, USA. E-mail: keckert@widecast.org

John W. Ferner Department of Biology, Thomas More College, Crestview Hills, KY 41017, USA. [Mailing address: Casa de los Lagartos, 2966 E. Placita Santa Lucia, Tucson, AZ 85716, USA.] E-mail: fernerjw@gmail.com

Robert N. Fisher U.S. Geological Survey, Western Ecological Research Center, San Diego Field Station, 4165 Spruance Road, Suite 200, San Diego, CA 92101, USA. E-mail: rfisher@usgs.gov

Nancy N. FitzSimmons Australian Rivers Institute, Griffith School of Environment, Griffith University, Nathan, QLD 4111, Australia. E-mail: n.fitzsimmons@griffith.edu.au

xxvi

| List of Contributors

Steve W. Gotte U.S. Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Museum Support Center, 4210 Silver Hill Road, Suitland, MD 27046, USA. E-mail: sgotte@usgs.gov

Brian Gratwicke Smithsonian’s National Zoological Park, Smithsonian Conservation Biology Institute, 3001 Connecticut Avenue NW, Washington, DC 20009, USA. E-mail: gratwickeb@si.edu

Robert W. Henderson Milwaukee Public Museum, 800 W. Wells St., Milwaukee, WI 53233, USA. E-mail: rh@mpm.edu

Brian T. Henen Post Office Box 1676, Twentynine Palms, CA 92277, USA. E-mail: bthenen@yahoo.com

Margaretha D. Hofmeyr Biodiversity and Conservation Biology Department, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa. E-mail: mdhofmeyr@uwc.ac.za

Jeremy F. Jacobs Department of Vertebrate Zoology, National Museum of Natural History, Museum Support Center, 4210 Silver Hill Road, Suitland, MD 27046, USA. E-mail: jacobsj@si.edu

Elliott R. Jacobson College of Veterinary Medicine, University of Florida, Gainesville, FL 32610, USA. E-mail: jacobsone@ufl.edu

Bruce A. Kingsbury Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, IN 46805, USA; E-mail: Bruce.Kingsbury@ipfw.edu

Gunther Köhler Senckenberg Forschungsinstitut und Naturmuseum, Senckenberganlage 25, 60325 Frankfurt a.M., Germany. E-mail: gkoehler@senckenberg.de

Pilar Lopez Departamento de Ecologia Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, Jose Gutierrez Abascal 2, 28006 Madrid, Spain. E-mail: pilar.lopez@mncn.csic.es

Luca Luiselli Environmental Studies Centre Demetra, via Olona 7, I-00198 Rome, Italy. E-mail: lucamlu@tin.it

Darryl I. MacKenzie Proteus Wildlife Research Consultants, P.O. Box 7, Outram 9062, New Zealand. E-mail: darryl@proteus.co.nz

Marco Mangiacotti Museo Civico di Storia Naturale di Milano, Corso Venezia, 55, 20121 Milan, Italy. E-mail: marco.mangiacotti@gmail.com

Charlie Manolis Wildlife Management International, P.O. Box 530, Karama, NT 0813, Australia. E-mail: cmanolis@wmi.com.au

Jose Martín Departamento de Ecologia Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, Jose Gutierrez Abascal 2, 28006 Madrid, Spain. E-mail: Jose.Martin@mncn.csic.es

Lindsay Renick Mayer Global Wildlife Conservation, P.O. Box 129, Austin, TX 78767, USA. E-mail: renickmayer@gmail.com

List of Contributors | xxvii

Earl D. McCoy Department of Integrative Biology, University of South Florida, Tampa, FL 33620, USA. E-mail: edm@mail.usf.edu

Stephen J. Mullin Department of Biology, Stephen F. Austin State University, Nacogdoches, TX 75962, USA. E-mail: sjmullin@sfasu.edu

Henry R. Mushinsky Department of Integrative Biology, University of South Florida, Tampa, FL 33620, USA. E-mail: mushinsk@usf.edu

Matthew Neff Smithsonian’s National Zoological Park, Reptile Discovery Center, 3001 Connecticut Avenue NW, Washington, DC 20009, USA. E-mail: NeffM@si.edu

David A. Pike College of Marine and Environmental Sciences, James Cook University, Townsville, QLD 4811, Australia. [Mailing address: 5108 Holland Avenue, Tampa, FL 33617, USA.] E-mail: david.pike22@gmail.com

Michael V. Plummer Department of Biology, Box 12251, Harding University, Searcy, AR 72149, USA. E-mail: plummer@harding.edu

Viorel D. Popescu Ohio University, Biological Sciences, 107 Irvine Hall, Athens, OH 45701, USA. E-mail: popescu@ohio.edu

Robert Powell Department of Biology, Avila University, 11901 Wornall Road, Kansas City, MO 64145, USA. E-mail: Robert.Powell@avila.edu

Arne R. Rasmussen

School of Conservation Esplanaden 34, 1263 København K,

Denmark. E-mail: arr@kadk.dk

Nathan J. Robinson The Leatherback Trust, Golding-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica. E-mail: nathanjackrobinson@gmail.com

J. Andrew Royle USGS Patuxent Wildlife Research Center, 12100 Beech Forest Road, Laurel, MD 20708, USA. E-mail: andy_royle@usgs.gov

Sharon Ryan Smithsonian Tropical Research Institute, Apartado Postal 0843–03092, Panamá, República de Panamá. E-mail: RyanSM@si.edu

Roberto Sacchi Dipartimento di Scienze della Terra e dell’Ambiente, Università di Pavia, 27100 Pavia, Italy. E-mail: roberto.sacchi@unipv.it

Marco Sannolo CIBIO, Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas N.7, 4485-661 Vairão, Vila do Conde, Portugal. E-mail: marco.sannolo@gmail.com

Stefano Scali Museo Civico di Storia Naturale di Milano, Corso Venezia, 55, 20121 Milan, Italy. E-mail: stefano.scali@comune.milano.it

Richard A. Seigel Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252, USA. E-mail: rseigel@towson.edu

Jennifer Sevin Center for Leadership in Global Sustainability, 900 North Glebe Road, Arlington, VA 22203, USA. E-mail: jennifer.sevin@gmail.com

Seth Stapleton Jumby Bay Hawksbill Project, Jumby Bay, P.O. Box 243, St. John’s, Antigua, West Indies. [Mailing address: 1317 Juno Ave., St. Paul, MN 55116, USA.] E-mail: seth@jbhp.org

xxviii

| List of Contributors

Joanna Sumner Museum Victoria, GPO Box 666, Melbourne, VIC 3001, Australia. E-mail: jsumner@museum.vic.gov.au

Chris Sutherland Department of Environmental Conservation, University of Massachusetts Amherst, Amherst, MA 01379, USA. E-mail: csutherland@umass.edu

Christopher R. Tracy Department of Biological Sciences, California State University Fullerton, 800 N. State College Blvd., Fullerton, CA 92831, USA. E-mail: ctracy@fullerton.edu

C. Richard Tracy Department of Biology, MS-315, University of Nevada, Reno, Reno, NV 89557, USA. E-mail: dtracy@unr.edu

Laurie J. Vitt Sam Noble Museum, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA. E-mail: vitt@ou.edu

Richard C. Vogt INPA/CBIO, Av. André Araújo, nº 2.936, Petrópolis, CEP 69.067– 375, Manaus, Amazonas, Brazil. E-mail: vogt@inpa.gov.br

John D. Willson Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA. E-mail: jdwillson@uark.edu

Marco A.L. Zuffi Museo Storia Naturale di Pisa, Università di Pisa, Via Roma 79, 56011 Calci (Pisa), Italy. E-mail: marco.zuffi@unipi.it

George R. Zug Department of Vertebrate Zoology-MRC162, National Museum of Natural History, P.O. Box 37012, Washington, DC 20013, USA. E-mail: zugg@si.edu

Part 1

Introduction

1

Reptile diversity and life history

Laurie J. Vitt

1.1 Introduction

The two most fundamental pieces of information necessary to begin developing eco- logical studies and conservation strategies for reptiles (or any organisms) are identifying the species and knowing what a species does in its natural habitat. Identifying species requires knowledge of other species or populations, particularly those that are closely related and may appear similar to the species or population of concern. The advent of Linnaean taxonomy provided a useful means of cataloguing species such that estimates of the number of species in various ‘taxonomic’ groups could be determined. When Systema Naturae was published in 1735 (Linnaeus, 1735) establishing a taxonomic hierarchy of names (classes, orders, genera, and species), the notion that evolution by natural selection occurred was 124 years in the future (Darwin, 1859), and the mech- anism underlying evolution by natural selection would not appear until 131 years later (Mendel, 1866). We now recognize that Linnaean taxonomy in its basic form does not accurately represent evolution and it has been replaced with evolutionary taxonomies. Learning what a species or population does in its natural habitat can be a challenge, particularly for species that are rare. I briefly review both reptile ‘diversity’ and life his- tories as a baseline for the following chapters that provide specific information on how to approach studies of these fascinating animals.

1.2 Reptile ‘diversity’

1.2.1 ‘Diversity’

The term ‘diversity’ has had several meanings in evolutionary biology and ecology and is often used loosely by professional biologists, land managers, and the general public. Technically speaking, when we are talking about the number of species in a given region, on a global level, or within a particular clade (evolutionary group with a common ances- tor), we are really talking about species richness (see Chapter 21). Species diversity, as used in ecology, incorporates relative abundance of each species.

1.2.2 Evolutionary history and numbers of reptile species

Extant reptiles are amniotes (i.e. they have an amniotic membrane in their embryo). Mammals are also amniotes and birds are nested within reptiles (Figure 1.1). Turtles

Reptile Ecology and Conservation. Edited by C. Kenneth Dodd, Jr. © Oxford University Press 2016. Published 2016 by Oxford University Press.

4

| Reptile diversity and life history

Testudines Crocodylia Aves Rhynchocephali a Sq uamat a Ma mmalia
Testudines
Crocodylia
Aves
Rhynchocephali a
Sq uamat a
Ma mmalia

Figure 1.1 Phylogeny of extant amniote tetrapod vertebrates.

and tortoises are now considered as sister to the Crocodylia–Aves (bird) clade, and the positions of some turtle families have changed (Figure 1.2). Based on a large number of molecular studies, it has become clear that both snakes and amphisbaenians are mono- phyletic clades nested within ‘lizards’ and thus the classic division of squamates into three suborders (Amphisbaenia, Serpentes, and Lacertilia) does not reflect the evolu- tionary history of these animals (Figure 1.3).

Crocodylian Families

Gavialidae Crocodylidae Alligatoridae Turtle Families Podocnemididae Pelomedusidae Chelidae Carretochelyidae
Gavialidae
Crocodylidae
Alligatoridae
Turtle Families
Podocnemididae
Pelomedusidae
Chelidae
Carretochelyidae
Trionychidae
Cheloniidae
Dermochelyidae
Chelydridae
Dermatemydidae
Kinosternidae
Testudinidae
Geoemydidae
Platysternidae

Emydidae

Figure 1.2 Phylogeny of extant crocodilian and turtle families based on molecular studies (see Vitt and Caldwell, 2014, for original references).

Reptile ‘diversity’ | 5

‘Lizards’ Amphisbaenians Dibamida e Bl anidae Diplodactylida e Cadeidae Carphodactylidae Bipedida e
‘Lizards’
Amphisbaenians
Dibamida e
Bl anidae
Diplodactylida e
Cadeidae
Carphodactylidae
Bipedida e
Pygopodidae
Trogonophidae
Eublepharidae
Amphisbaenidae
Gekkonidae
Rhineurida e
Phyllodactylidae
Sn akes
Sphaerodactylidae
(Serpentes)
Cord ylidae
Gerrhosauridae
Xantusiidae
Scincida e
Amphisbaenia
Lacertida e
Gymnophthalmidae
Ty phlopidae
Teiidae
Xenotyphlopidae
Anguidae
Anniellida e
Diploglossida e
Xenosauridae
Helodermatida e
Shinisaurida e
Lanthanotidae
Va ranidae
Chamaeleonidae
Agamidae
Ph ry nosomatida e
Gerrhopilidae
Leptotyphlopidae
Anomalepididae
Aniliidae
Tropidophiidae
Loxocemidae
Pythonidae
Xenopeltidae
Uropeltida e
Boidae
Iguanidae
Calabariidae
Crotaphytidae
Bolyriidae
Leiocephalida e
Xenophiidae
Polychrotidae
Ac rochordida e
Cory tophanidae
Xenodermatidae
Dactyloida e
Pa reatidae
Tropidurida e
Viperidae
Hoplocercidae
Ho malopsida e
Liolaemida e
Lamprophiidae
Leiosaurida e
El apidae
Opluridae
Serpentes
Colubridae

Figure 1.3 Phylogeny of extant lizard, amphisbaenian, and snake families based on molecular studies (see Vitt and Caldwell, 2014, for original references).

As of March 2015, 10,178 species of living non-avian reptiles were known, and new species are being described regularly (Uetz and Hošek, 2014). Of these, 341 are turtles or tortoises, 25 are crocodilians, 1 is a rhynchocephalian (some consider Sphenodon to consist of two species), and the remainder are squamates (Table 1.1). Among squa- mates, 6040 are what we typically refer to as lizards, 3522 are snakes, and 190 are amphisbaenians.

1.2.3 Morphological and ecological diversity

So, what are these animals that we typically call reptiles, how do the major groups differ, and how variable morphologically, behaviourally, and ecologically are species within

6

| Reptile diversity and life history

Table 1.1 Taxonomic diversity of reptiles

Major clade

Families

Genera

Species

Turtles Crocodilians Squamate ‘lizards’ Squamate amphisbaenians Squamate ‘snakes’ Rhynchocephalians

14

95

341

3 (4)

9

25

36

533

6040

6

20

190

27

522

3522

1

1

1 (2)

Notes: Numbers of families, genera, and species are based on The Reptile Database (http:// www.reptile-database.org/). The potentially additional crocodilian family (Caimanidae) is based on Willis (2009) and some consider Sphenodon (Rhynchocephalia) to consist of two species.

each major group? Most people would easily distinguish a turtle from a crocodilian, and both of these from other extant reptiles. All turtles have shells consisting of a dorsal carapace and a ventral plastron. Relative size of the carapace and plastron varies greatly, and shell shape varies from very flat to high domes. Most shells are hard with distinct keratinized scales (called scutes), but some, like softshell turtles and the marine Leatherback Turtles, have softer shells lacking scutes. Turtles lack teeth, but have sharp keratinized ridges resting on their jawbones. Crocodilians are lizard-like in overall body form, but can easily be distinguished from all lizards by the absence of lips, an elongate snout, and exposed teeth that interlock. They also have a cloacal slit that runs parallel to the body, whereas lizards have a cloacal slit that runs perpendicular to the body. To most people, snakes would be easily distin - guishable from lizards because they have no limbs. However, loss of limbs has occurred independently a number of times within squamates, and only one of those times was in the ancestor to snakes (Wiens et al., 2006). For example, five of the six families of amphisbaenians lack limbs and the other family is represented by only three species, each of which has only small, mole-like front limbs. Consequently, absence of limbs is not the best trait for distinguishing a snake from a lizard. All snakes have spectacles over the eyes and no eyelids, but some lizards (e.g. certain gecko families, xantusiids, and oth- ers) also lack eyelids and have spectacles. Snakes have long forked tongues used to detect chemicals in the environment, but many lizards (e.g. varanids and helodermatids) also have long, forked tongues. Snakes lack external ear openings as do a few lizards (e.g. Cophosaurus and Holbrookia). Characters that distinguish lizards from snakes are for the most part skeletal, and thus not obvious. Nevertheless, the combination of long-forked tongue, spectacle over the eyes, lack of an external ear opening, and lack of limbs dis- tinguishes all snakes from nearly all lizards and amphisbaenians. Amphisbaenians are easily distinguished from other squamates by the ring-like pattern of scales around their bodies. The Tuatara is distinguished from all other extant reptiles by the combination of lack of a male copulatory organ, a cloacal slit that runs parallel to the body, and a beak- like structure in the front of the jaws. As a group, turtles have the widest global distribution among reptiles, largely because all species in two turtle families live in oceans. Freshwater and terrestrial turtles occur on

Reptile ‘diversity’ | 7

all continents except Antarctica, and a number of species occur at high latitudes (Vitt and Caldwell, 2014). Crocodilians for the most part are restricted to freshwater and estuarine habitats associated with tropical and subtropical landmasses, but the Estuarine Crocodile (Crocodylus porosus) can venture long distances into the oceans off Southeast Asia, the Philippines, and Papua New Guinea. In terms of climatic zones, squamates have the widest distribution occurring on all major continents except Antarctica, as well as many oceanic islands. A few species, such as the Viviparous Lizard (Zootoca vivipara), enter the Arctic Circle. Sea snakes (subfamily Hydrophinae) occupy continental shelf regions of the Pacific and Indian Oceans with one species reaching tropical areas along the western coast of Central and South America. Tuataras are restricted entirely to about 30 islands off the northeast coast of North Island and western Cook Strait of New Zealand. Turtles are diverse ecologically. Many species live in freshwater and feed primarily on invertebrates, although some emydid, carettochelyid, and chelid turtles are herbiv- orous. Map turtles (Graptemys) specialize on molluscs that they capture on river bot- toms. The large terrestrial tortoises (Testudinidae) are herbivorous. Sea turtles tend to be dietary specialists as adults, and different species specialize on different organisms. For example, Eretmochelys imbricata feeds on sponges and soft corals, Dermochelys coriacea feeds largely on gelatinous invertebrates such as jellyfish and salps, whereas Chelonia mydas feeds on marine grasses or algae. Crocodilians live primarily in water, all are relatively large bodied, and all feed on animals. The type and size of animals eaten depend a lot on body size—juvenile croco- dilians often feed on invertebrates as well as small vertebrates, whereas adults feed on ver- tebrates, some as large as they are, which are dismembered and torn apart. Crocodilians with long narrow snouts, such as the gavial, feed largely on fish. Squamates are so diverse ecologically that any generalizations are filled with excep- tions (Greene, 1997; Pianka and Vitt, 2003; Lillywhite, 2014). Snakes and lizards can be found in nearly every imaginable microhabitat. Many are arboreal, others terres- trial, others subterranean, some aquatic, and yet others are marine. Many are diurnal, whereas many others are nocturnal. Some are highly specific in their dietary choices, whereas others will eat nearly anything that moves. Much of the variation in ecological traits is clade or species specific (Cadle and Greene, 1993; Vitt et al., 2003; Vitt and Pianka, 2005). For example, snakes in the genus Dipsas are thin-bodied, typically arboreal, nocturnal, and specialize on snails and slugs, whereas snakes in the family Leptotyphlopidae live in ant and termite nests feeding on larvae. Lizards in the genera Phrynosoma, Plica, and Uracentron feed almost entirely on ants. Phrynosoma are strictly terrestrial whereas Plica and Uracentron are arboreal. With the exception of herbivor- ous lizards, nearly all lizards and all snakes swallow their prey whole. Predaceous lizards usually feed on arthropods or other invertebrates, although some of the large species, particularly in the families Helodermatidae, Varanidae, and Teiidae, frequently feed on vertebrates (Pianka and King, 2004; Beck, 2005). The Komodo Dragon (Varanus komodoensis) can mortally wound large prey including water buffalo, wait for them to die and begin rotting, and dismember them, swallowing large portions of the dead prey (Auffenberg, 1981). All snakes swallow their prey whole, but mechanisms for capturing

8

| Reptile diversity and life history

and killing prey vary from strike + constriction, simply biting and swallowing alive, to strike + envenomation.

1.3 Diversity of life histories

1.3.1 Definitions

The term ‘life history’ generally refers to a combination of the following traits: num- ber of offspring, frequency of reproduction, egg or offspring size, female size or age at first reproduction, reproductive life span, longevity, and age-specific survivorship. Additional variables, including nesting ecology, juvenile development, senescence, and parental investment, are often included (Williams, 1966; Stearns, 1992). Data on age- specific survivorship, reproductive life span, and senescence are not available for the vast majority of reptile species. Without this critical information, population reproductive rates (referred to as r, the intrinsic rate of population growth), potential replacement rates (R, in which a value of 1 indicates a stable population), and reproductive value (RV = current reproduction + residual reproductive value) cannot be calculated. These are among the most critical variables necessary to develop realistic long-term manage- ment programmes for species. Nevertheless, insight into the many different life histories exhibited by reptiles can serve as useful starting points.

1.3.2 General observations

All turtles, crocodilians, and the Tuatara deposit eggs (none are live-bearing) and are relatively long-lived and late maturing when compared with most squamates. All repro- duce sexually, and most have environmental sex determination (ESD) often referred to as temperature-dependent sex determination (TSD) (Valenzuela and Lance, 2004). Parental care exists in most if not all crocodilians and has been reported in several turtle species. Among squamates, a remarkable diversity of life histories exist, including both sexual and asexual reproduction, ESD in some, multiple independent origins of live- bearing, extended parental care in some, and a near-continuum from short-lived, early maturing species to long-lived and late maturing species.

1.3.3 Turtle life histories

All turtles reproduce sexually, do not guard or attend nests, most deposit eggs in nests dug into the ground, and species may or may not have sex chromosomes (Table 1.2). Heterogamety (presence of sex-determining chromosomes) occurs in some species (e.g. Trionychidae, Siebenrockiella crassicollis), but most lack sex chromosomes and exhibit TSD. TSD is believed to be ancestral in turtles, with gonadal sex determination (GSD) evolving at least six times independently (Warner and Janzen, 2010; Warner, 2011). Parental care of offspring is rare in turtles, reported in only three of the known 341 species.

1.3.4 Crocodilian life histories

All crocodilians reproduce sexually and females deposit eggs in nests constructed of vegetative debris (Graham and Beard, 1973; Thorbjarnarson, 1996). Parental care in

Diversity of life histories | 9

Table 1.2 Mechanisms of sex determination in reptiles

Genetic sex determination

Temperature-dependent sex determination

 

Heterogamety in

Heterogamety in

Homogamety

males (XY/XX)

females (ZZ/ZW)

Turtles

Chelidae,

Geomydidae,

Chelidae

Pelomedusidae,

Geomydidae,

Trionychidae

Podocnemididae,

Kinosternidae

Geomydidae,

 

Carettochelyidae,

Cheloniidae,

Chelydridae,

Dermatemydidae,

Dermochelyidae,

Emydidae,

Kinosternidae,

Testudinidae,

Trionychidae

Crocodilians

None

None

None

Alligatoridae,

 

Crocodylidae,

Gavialidae

Tuataras

None

None

None

Sphenodontidae

Squamates

Iguania,

Gekkonoidea,

Iguania,

Agamidae,

Gekkonoidea,

Lacertidae,

Gekkonoidea,

Diplodactylidae,

Teiidae,

Amphisbaenia,

Lacertidae,

Eublepharidae,

Scincidae

Varanidae,

Teiidae,

Gekkonidae,

 

Boidae,

Scincidae,

Scincidae

Colubridae,

Colubridae,

Elapidae,

Elapidae

Viperidae

Notes: Original sources can be found in Vitt and Caldwell (2014).

the form of nest attendance, freeing hatchlings from eggs, and carrying (in the mouth) hatchlings to water occurs in most species studied. Smaller species and individuals produce smaller clutches of eggs than larger species or individuals. For example, the relatively small (1.3 m adult snout–vent length (SVL)) Paleosuchus trigonotus typically produces about 15 eggs, whereas the large (2.7 m SVL) Crocodylus porosus can produce, on average, about 50 eggs. All studied crocodilians have ESD (Valenzuela and Lance, 2004). Nest temperatures near 31°C produce equal numbers of males and females. Temperatures of 30°C or lower produce females and nest temperatures of 32–33°C produce males. Age at sexual maturity and longevity vary among species, but relative to most squamates, all can be considered late maturing. For example, Gavials (Gavialis gangeticus) reach maturity in 15–18 years and American Alligators (Alligator mississip- piensis) reach maturity in 7–10 years.

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| Reptile diversity and life history

1.3.5 Squamate life histories

Squamates (lizards and snakes) exhibit remarkable life history variation, and much of the overall variation is historical (e.g. correlated with phylogeny) (Dunham et al., 1988; Mesquita and Colli, 2010). Variation in some traits, such as egg or offspring size and number, is often associated with species body size, and egg or offspring number is usu- ally associated with female size within species. Nevertheless, in some clades, such as Dactyloidae, Phyllodactylidae, and Sphaerodactylidae, clutch size is one egg and eggs are produced in rapid succession. In some other clades, such as Anniellidae, Gekkonidae, Diplodactylidae, Carphodactylidae, and Eublepharidae, females produce clutches or litters of only two. Larger varanids (e.g. Varanus bengalensis) can produce clutches of 40 or more eggs. The largest species of pythons and boas can produce upwards of 100 eggs or 60 offspring, respectively. Most squamates produce eggs (oviparity), but 20% of squamate species are live-bearing (viviparous). Frequency of reproduction varies greatly across clades, but appears to be constrained by temperature, at least at higher elevations and latitudes. For example, some tropical Anolis can produce an egg every seven days whereas most Temperate-zone squamates produce one or two clutches per year. Most viviparous squamates produce a single litter per year, and some tropical egg-laying squamates (e.g. Polychrus acuirostris) also produce only a single clutch each year. Because many of the more interesting aspects of squamate life histories cut across taxa, I briefly summarize these rather than providing details on a taxon-by-taxon basis (but see Fitch, 1970, and Vitt and Caldwell, 2014, for additional summaries).

• Parthenogenesis is the production of offspring by females without involvement of males and is cloning given that offspring produced are genetically identical to their mothers. Parthenogenesis was first discovered in the lizard Darevskia saxicola by Illya Darevsky (1958). Parthenogenesis has since been confirmed by (1) lack of males in populations, (2) rearing females from birth until they produced off- spring, (3) immunocompatibility (skin grafting) experiments, (4) chromosome studies, and (5) genetic studies. More than 50 squamate species are partheno- genetic, and in nearly all cases, parthenogenetic species arose via hybridization between two sexual species or back-crossing between a parthenogenetic species and a sexual one (Reeder et al., 2002). Diploid and triploid parthenogens are most common, but one (Aspidoscelis neavesi) is tetraploid (Cole et al., 2014). The xan- tusiid lizard Lepidophyma flavimaculatum appears to be an exception in that it is not a hybrid species (Sinclair et al., 2010). Parthenogenesis occurs in eight lizard families (Agamidae, Chamaeleonidae, Gekkonidae, Gymnophthalmidae, Teiidae, Lacertidae, Xantusiidae, and Scincidae) and one snake family (Typhlopidae). In addition, females of a small number of normally sexually reproducing species (e.g. Nile Monitors, Komodo Dragons, Indian Pythons, and Sierra Gartersnakes) have produced offspring in captivity in the absence of males. The ecological significance of parthenogenesis in reptiles remains a mystery (Kearney et al., 2009), but the short-term advantage is that it increases reproductive rate because every individual produced is a reproducing female.

Diversity of life histories | 11

• Viviparity refers to live birth, and among extant reptiles, occurs only in squamates. Although relatively uncommon even in squamates, viviparity has arisen at least 114 times, which is by far the greatest number of independent origins known for tetrapod vertebrates (e.g. Blackburn, 1982, 1985, 2000). The primary advantage of viviparity is that it allows the parental female to exert some control over incu- bation temperatures via behavioural thermoregulation. Because most viviparous species live in areas with cool climates (high elevations or latitudes), adaptation to cold climates appears to best explain most origins of viviparity (Shine and Berry, 1978; Shine, 1985, 2002). The primary disadvantage is that because females must carry their offspring during the entire incubation period, and because the add- itional weight of the embryos impacts locomotion, females can incur increased risk during pregnancy. Because of the many origins of viviparity, it does not occur in the same way in all viviparous species. Many species simply hold fully yolked eggs in the oviduct until development is complete (e.g. the snake Opheodrys vernalis). Others provide various degrees of embryonic nourishment to developing offspring. Depending upon species, squamate placentae vary both morphologically and in the degree to which they supply nutrients to developing embryos (Blackburn et al., 1984; Qualls et al., 1997).

• Parental care is rare, or at least poorly known in squamates. Forty-one species of lizards and 47 species of snakes exhibit some form of parental care. Parental care in squamates varies from aiding neonates out of placental membranes at birth, cre- ating nests and attending or brooding eggs until they hatch, to defending nests or allowing juveniles to remain in adult territories. A remarkable example of brooding occurs in some pythons, which not only brood their eggs until they hatch, but ele- vate temperatures of the nest and eggs by shivering thermogenesis (Somma, 2003).

• Among squamates, at least four mechanisms of sex determination are recognized (Table 1.2; Warner and Janzen, 2010; Warner, 2011). Three of these are genetic (i.e. GSD): heterogamety in males (XY/XX), heterogamety in females (ZZ/ZW), and homogamety (sex chromosomes undifferentiated). The fourth is TSD, in which narrow ranges of temperature variation can shift the hatchling sex ratio. Although TSD is most common in species lacking differentiated sex chromo- somes, it occurs in some species with heteromorphic sex chromosomes. Moreover, elements of GSD and TSD are known to occur within species and populations, and sex reversal has even been shown to trigger the rapid transition from GSD to TSD (Holleley et al., 2015). Teasing out the adaptive significance of TSD (or ESD) has been elusive, but experiments with the agamid lizard Amphibolurus muricatus revealed that fitness of each sex was maximized by the incubation temperature that produced each sex, just as theory had predicted (Warner and Shine, 2008).

1.3.6 Tuatara life history

Tuataras reproduce sexually, females deposit 5–15 eggs in shallow nest cavities that they dig, and hatching occurs 11–16 months later with development arrested during winter. Females nest once every four years and eggs are carried in the oviducts for 6–8 months

12

| Reptile diversity and life history

prior to deposition (Cree et al., 1992; Cree, 2002, 2014). This unique reproductive pat- tern is thought to be an adaptation to the cool environment on islands of New Zealand where the Tuatara occurs. Unlike other extant reptiles, male tuataras do not have a copu- latory organ. Sperm transfer is accomplished by cloacal apposition, similar to birds. TSD occurs, with developmental temperatures of 21°C producing equal numbers of males and females, 22°C producing mostly males, and 20°C producing mostly females. Nevertheless, both genetic and environmental factors can be involved in tuatara sex determination (Cree et al., 1995). Tuataras also grow more slowly than other reptiles, continuing to grow in size during the first 35 years of their lives. Tuataras are extremely long-lived, with individuals known to reach more than 100 years in age (Anonymous, 2009). Tuataras reach sexual maturity at an age of 10–20 years.

1.4 Summary

Extant reptiles constitute a taxonomically, morphologically, and ecologically diverse group of tetrapods. They occur on all continents except Antarctica and can be found in nearly every possible habitat, including some that might be considered extreme for animals that depend on behavioural adjustments to gain and lose heat. A few occur within the Arctic Circle, an entire clade of snakes (sea snakes) occurs in continental shelf regions of the oceans, and many other species live nearly exclusively underground. The diversity of life histories among reptiles is also impressive, although most of that diver- sity occurs only in squamates. From an ecological and conservation perspective, it seems clear that no single model can be applied to reptiles. Rather, detailed natural history data are necessary to deter- mine factors that might lead to persistence or extirpation of local populations. Ideally, age-specific survivorship schedules determined over long time periods (at least one cohort’s lifespan) should provide data necessary to determine whether populations are stable, increasing, or decreasing. Unfortunately, these data exist for but a handful of species. Often observations on a single life-history trait can influence development of conservation strategies. For example, if freshwater turtles deposit their eggs 200 m from the ponds they live in, then those nesting areas must be included in the turtle’s manage- ment programme. Likewise, head-start programmes for sea turtles should incorporate incubation temperatures that maximize fitness for each sex. The reactionary approach to conservation that is often tied to funding (if it isn’t broken, don’t fix it, but when it breaks, throw a large amount of money at it) is unrealistic when it comes to reptile conservation. In most cases we don’t have pre-disturbance data, rendering it nearly impossible to (a) determine whether a population is actually declining and (b) what to do about it. Because we lack long-term monitoring data for a vast majority of reptile species, we often cannot be certain whether it is normal for populations to vary dramat- ically through time. We already know this is true for North American amphibians, but comparable data do not exist for most reptile species. Moreover, conservation funding is often biased towards large, highly visible species such as sea turtles, crocodilians, and the tuatara, even though large numbers of small-bodied squamates are on the decline (e.g. Sinervo et al., 2010).

Summary | 13

References

Anonymous. (2009). Tuatara becomes a father for the first time, aged 111. New Zealand Herald Available at: http://www.nzherald.co.nz/nz/news/article.cfm?c_id=1&objectid=10553616. Auffenberg, W. (1981). The Behavioral Ecology of the Komodo Dragon . Gainesville, FL: University Presses of Florida. Beck, D.D. (2005). Biology of Gila Monsters and Beaded Lizards. Berkeley, CA: University of California Press. Blackburn, D. (1982). Evolutionary origins of viviparity in the Reptilia. I. Sauria. Amphibia- Reptilia, 3, 185–205. Blackburn, D. (1985). Evolutionary origins of viviparity in the Reptilia. II. Serpentes, amphis- baenia, and ichthyosauria. Amphibia-Reptilia, 6, 259–91. Blackburn, D.G. (2000). Reptilian viviparity: past research, future directions, and appropriate models. Comparative Biochemistry and Physiology Part A, 127, 391–409. Blackburn, D.G., Vitt, L.J., and Beuchat, C.A. (1984). Eutherian-like reproductive specializa- tions in a viviparous reptile. Proceedings of the National Academy of Sciences USA, 81, 4860–3. Cadle, J.E., and Greene, H.W. (1993). Phylogenetic patterns, biogeography, and the ecologic- al structure of Neotropical snake assemblages. In R.E. Ricklefs and D. Schluter (eds) Species Diversity in Ecological Communities: Historical and Geographical Perspectives. Chicago, IL:

University of Chicago Press, pp. 281–93. Cole, C.J., Taylor, H.L., Baumann, D.P., et al. (2014). Neaves’ Whiptail Lizard: the first known tetraploid parthenogenetic tetrapod (Reptilia: Squamata: Teiidae). Breviora, 539, 1–20. Cree, A. (2002). Tuatara. In T. Halliday and K. Adler (eds) The New Encyclopedia of Reptiles and Amphibians. Oxford: Oxford University Press, pp. 210–11. Cree, A. (2014). Tuatara. Biology and Conservation of a Venerable Survivor. Christchurch, NZ:

Canterbury University Press. Cree, A., Cockrem, J.F., and Guillette, L.J., Jr. (1992). Reproductive cycles of male and female tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. Journal of Zoology, 226,

199–217.

Cree, A., Thompson, M.B., and Daugherty, C.H. (1995). Tuatara sex determination. Nature, 375, 543. Darevsky, I.S. (1958). Natural parthenogenesis in certain subspecies of rock lizard, Lacerta saxi- cola Eversmann. Doklady Akademii Nauk SSSR Biological Science, 122, 877–9. Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. London: John Murray. Dunham, A.E., Miles, D.B., and Reznick, D.N. (1988). Life history patterns in squamate rep- tiles. In C. Gans and R.B. Huey (eds) Biology of the Reptilia, Volume 16. Ecology B. Defense and Life History. New York: A. R. Liss, pp. 441–552. Fitch, H.S. (1970). Reproductive cycles in lizards and snakes. Miscellaneous Publications of the Museum of Natural History of the University of Kansas, 52, 1–247. Graham, A., and Beard, P. (1973). Eyelids of Morning. The Mingled Destinies of Crocodiles and Men. Greenwich, CT: New York Graphic Society, Ltd. Greene, H.W. (1997). Snakes. The Evolution of Mystery in Nature. Berkeley, CA: University of California Press. Holleley, C.E., O’Meally, D.O., Sarre, S.D., et al. (2015). Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature, 523, 79–82. Kearney, M., Fujita, M.K., and Ridenour, J. (2009). Lost sex in the reptiles: constraints and cor- relations. In I. Schön, K. Martens, and P. van Dijk (eds) Lost Sex, The Evolutionary Biology of Parthenogenesis. Dordrecht: Springer, pp. 447–74. Lillywhite, H.B. (2014). How SnakesWork. Structure, Function, and Behavior of theWorld’s Snakes. Oxford: Oxford University Press.

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Linnaeus, C. (1735). Systema Naturae, sive regna tria naturae systematice proposita per classes, ordines, genera, & species. Leiden: Haak, pp. 1–12. Mendel, G. (1866). Versuche über Plflanzen-hybriden.Verhandlungen des naturforschenden Vereins. Brünn, IV, 3–47. Mesquita, D.O., and Colli, G.R. (2010). Life history patterns in tropical South American liz- ards. In O.H. Gallegos, F.R.M. Cruz, and J.F.M. Sánchez (eds) Reproduccíón en Reptiles:

Morphologia, Ecología, y Evolución. Mexico: Universidad Autónoma del Estado de México, pp. 45–71. Pianka, E.R., and King, D.R. (eds) (2004). Varanoid Lizards of the World. Bloomington, IN:

Indiana University Press. Pianka, E.R., and Vitt, L.J. (2003). Lizards. Windows to the Evolution of Diversity. Berkeley, CA:

University of California Press. Qualls, C.P., Andrews, R.M., and Mathies, T. (1997). The evolution of viviparity and placenta - tion revisited. Journal of Theoretical Biology, 185, 129–35. Reeder, T.W., Cole, C.J., and Dessauer, H.C. (2002). Phylogenetic relationships of whiptail lizards of the genus Cnemidophorus (Squamata: Teiidae): a test of monophyly, reevaluation of karyotypic evolution, and review of hybrid origins. American Museum Novitates, 3365,

1–61.

Shine, R. (1985). The evolution of viviparity in reptiles: an ecological analysis. In C. Gans and F. Billett (eds) Biology of the Reptilia. New York: John Wiley and Sons, pp. 677–80. Shine, R. (2002). An empirical test of the ‘predictability’ hypothesis for the evolution of viviparity in reptiles. Journal of Evolutionary Biology, 15, 553–60. Shine, R., and Berry, J.F. (1978). Climatic correlates of live-bearing in squamate reptiles. Oecologia, 33, 261–8. Sinclair, E.A., Pramuk, J.B., Bezy, R.L., et al. (2010). DNA evidence for nonhybrid origins of parthenogenesis in natural populations of vertebrates. Evolution, 64, 1346–57. Sinervo, B., Méndez-de-la-Cruz, F., Miles, D.B., et al. (2010). Rapid erosion of lizard diversity at global scales: altered thermal niches due to climate change. Science, 328, 894–9. Somma, L.A. (2003). Parental Behavior in Lepidosaurian and Testudinian Reptiles. Malabar, FL:

Krieger Publishing Company. Stearns, S.C. (1992). The Evolution of Life Histories. Oxford: Oxford University Press. Thorbjarnarson, J. (1996). Reproductive characteristics of the order Crocodylia. Herpetologica, 52, 8–24. Uetz, P., and Hošek, J. (eds) (2014). The Reptile Database. Available at: http://www.reptile- database.org/. Valenzuela, N., and Lance, V. (eds) (2004). Temperature-Dependent Sex Determination in Vertebrates. Washington, DC: Smithsonian Books. Vitt, L.J., and Caldwell, J.P. (2014). Herpetology: An Introductory Biology of Amphibians and Reptiles. 4th ed. San Diego, CA: Academic Press. Vitt, L.J., and Pianka, E.R. (2005). Deep history impacts present-day ecology and biodiversity. Proceedings of the National Academy of Sciences USA, 102, 7877–81. Vitt, L.J., Pianka, E.R., Cooper, W.E., Jr., et al. (2003). History and the global ecology of squa- mate reptiles. American Naturalist, 162, 44–60. Warner, D.A. (2011). Sex determination in reptiles. In D.O. Norris and K. Lopez (eds) Hormones and Reproduction of Vertebrates, Volume 3. Reptiles. San Diego, CA: Academic Press, pp. 1–38. Warner, D.A., and Janzen, F.J. (2010). Diversity of sex-determining mechanisms. In D. Westneat and C.W. Fox (eds) Evolutionary Behavioral Ecology. Oxford: Oxford University Press, pp. 81–3.

Summary | 15

Warner, D.A., and Shine, R. (2008). The adaptive significance of temperature-dependent sex determination in a reptile. Nature, 451, 566–8. Wiens, J.J., Brandley, M.C., and Reeder, T.W. (2006). Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution, 60,

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Williams, G.C. (1966). Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton, NJ: Princeton University Press. Willis, R.E. (2009). Transthyretin gene (TTR) intron 1 elucidates crocodylian phylogenetic rela- tionships. Molecular Phylogenetics and Evolution, 53, 1049–54.

2

Planning and setting objectives in field studies

Robert N. Fisher

2.1 Introduction

The objective of this chapter is to engage the researcher in the logic steps required to design and plan field studies on the ecology and conservation of reptiles. I previously described the approaches needed to design inventory and monitoring programmes for reptiles (Fisher and Mitrovich, 2012; see also Cogălniceanu and Miaud, 2010); most of the information provided in these publications is applicable here. Here, however, I expand the focus from ecology to conservation techniques, many of which become management actions designed to recover or maintain at-risk species or populations. Often these techniques involve a higher level of uncertainty and risk than inventory and monitoring techniques, which vary from observational to highly quantitative, but involve the tenet of ‘do no harm’. Setting goals for management may be straightforward, but developing objectives can be less straightforward as it often involves decisions that are uncomfortable to make and difficult to implement as a result of this additional risk. It is often much easier to make no decision than to make one that might result in harm to an at-risk species. Unfortunately, even ‘no decision’ is a decision when it comes to con- servation (Meek et al., 2015). First, I’ll review the difference between goals and objec- tives and then discuss how we implement field studies and/or management actions.

2.2 Planning: goals versus objectives

Goals are descriptions of what one intends to accomplish. These are typically not direct- ly actionable, but serve as the larger vision for the study or set of actions that will follow. For instance, goals might be to:

• Determine the diversity of reptiles of some geographically defined area.

• Conserve x, y, or z species and their habitats.

• Identify the covariates driving the distribution of certain species.

• Increase the abundance of a certain species.

These goals seem relatively simple and straightforward, but they give no guidance on the steps to be taken or how to implement them, track progress, or follow timelines. This is the function of objectives. Objectives are the measurable steps required to achieve the established goals. They are the strategic activities developed during the planning

Reptile Ecology and Conservation. Edited by C. Kenneth Dodd, Jr. © Oxford University Press 2016. Published 2016 by Oxford University Press.

Design

|

17

Table 2.1 Examples and definitions of goals and objectives

 

Goal

Objective

Meaning

General purpose of the endeavour

Something that can be attained or accomplished; typically a target We need to remove all invasive California Kingsnakes from the Canary Islands Specific action that supports goal accomplishment Must be tangible Short term

Example

We want to maintain biodiversity in the Canary Islands

Action

Outcome for which we strive to attain

Measure

Goals might not be measurable Longer term

Time frame

of a project and are tied to available resources and a specific time frame. Objectives should be SMART—specific, measurable, attainable, realistic/relevant, and timed/time bound (Schroeder, 2009). Many online tools are available to help one define objectives and evaluate whether they are SMART or not (example URLs are listed at end of this chapter). Meeting a specific goal may require many objectives. It may not be possible to define some of them until certain experiments have been conducted; often evaluations of sampling protocols are needed to increase certainty in the biological results. Examples of objectives might be:

• Test traps to verify that they effectively sample all life classes of a certain species during the first year.

• Review and, if necessary, develop marking techniques for uniquely identifying a certain species during the first month.

• Measure covariates of trapping stations using quantitative sampling during the first spring.

Additional definitions and examples are in Table 2.1.

2.3 Design

Time and/or money are never sufficient to conduct a complete, ideal project. Projects almost always are more complex than originally realized. Biological assumptions are typically flawed and need to be reassessed throughout a project. The best way to deal with uncertainties is to maximize the scope and intent when formulating a project and setting goals so that a certain level of failure can be absorbed. This allows one to push beyond safe boundaries (a conservative design) that might not ultimately lead to project success. A key design element is identifying the minimum accomplishment required to achieve success. Phases that equate to milestones that meet some success criteria should be clearly built into the objectives. Having more objectives than possible to accomplish with the available time and resources will create complexity, challenging the researcher to evaluate and prioritize actions continually, but it will also enhance the significance of

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| Planning and setting objectives in field studies

a project in the end. Conceptual models used to visualize this complexity and identify

critical uncertainties are discussed in Section 2.4. An additional key element of a successful project is balancing elegant design and functional design. Involving statisticians in the project design is critical to success, but can also lead to a study that is biologically irrelevant or impossible to carry out. Because so many uncertainties (i.e. knowing the number of replicates, sample sizes, or repeat vis- its required, or logistical difficulties) exist at the onset of a project, designing it may seem

difficult (or even impossible) and thus lead to design paralysis. It is possible to model some parameters initially and run power analyses to estimate what some sample sizes might need to be, and how many replicates are required, as a first way to deal with uncer- tainty. At this point it is important to consider functional design and adaptive design. The concept of functional design is that as the data are collected in a way that there are multiple independent elements, such that once a design is implemented if it needs to be changed or modified, or some sampling is unfeasible, not all parts of the design are impacted. Adaptive design is where changes in sampling are informed by the data being collected. This approach typically serves to make studies more efficient (such as fewer days, shorter transects) while meeting or exceeding study objectives. Knowing the type of study design at the beginning will allow a researcher to better understand what parts of the design are flexible, and what parts are fixed, such that if they change, the study will not be successful. Asking the initial question ‘What is really important in this study? ’ fol-

lowed by ‘Is it a statistical trend? Is it successful reproduction? Is it demographic?’ will better define the relevant design approach. A study that determines that there are other ways to measure and implement sampling that meets the objectives and still has a reasonable chance of success would be adaptive, but not necessarily elegant. Sometimes simpler sampling procedures with more replication will result in a more straightforward dataset to interpret and analyse. One critical way to think about design is in the dichotomy between verifying trends that are obvious versus forcing statistics to extract trends from patterns that are unclear. Utilizing robust sampling frames with statistical inference is not the same as utilizing complex measurements on the ground. An example of this contrast might be having many plots stratified across habitat types that are coarsely defined utilizing existing GIS layers. Let’s say the scale of the vegetation layer is 1 ha, which means that there has been

a category of vegetation assigned to each 1 ha pixel of the GIS layer. If the sampling

plots are 50 m wide and the region being sampled is 500 km 2 , then you can have a very robust sampling frame with replication across vegetation categories and random plot placement. Statistically robust trends might be determined from this design regarding vegetation and species of interest, and this might well answer one set of questions. If the species or community is responding to soil texture (rock size) and there is a gen- eral relationship between vegetation and soil texture, however, then this relationship might be missed. If complex measurements are taken of vegetation and soil at the plot scale (50 m) to describe the local heterogeneity within and between plots, then a differ- ent set of relationships might emerge, answering a different set of questions. Thinking through which of these questions is more important to managers or management will inform which approach to utilize when conducting the study, even though both might

Conceptual models | 19

be statistically robust. That said, researchers want to eliminate observer bias as much as possible when sampling; incorporating procedures that minimize ambiguity in species identification or measurement (during trapping or other sampling, as vouchers) is thus an important consideration.

2.4 Conceptual models

One way to address uncertainty when dealing with complex issues is to use conceptual models to direct goals, objectives, and, ultimately, study design (Atkinson et al., 2004). Conceptual models are based on literature reviews and serve as visual depictions of the relationships between variables that describe a system of interest. Example systems could be a vernal pool ecosystem or the life history of a given species of reptile. For a vernal pool, the model might include all of the species using the pool for recruitment, the predator–prey relations between them, the timing of water availability, and the upland context of the pool system in driving diversity or species density. For a single

species, a model might focus on critical reproductive traits, various mortality factors at different life stages, and individual movement requirements for territoriality or mate selection. Conceptual models vary in complexity and rigour depending on the questions being asked and the amount of pre-existing knowledge of the system. Substantial literature on development and use of conceptual models, which ‘simultaneously need to embrace and deconstruct contextual complexity’, is available (Margoluis et al., 2009). When

a system is minimally known or primarily understood through expert opinion, the

models can initially be quite simplistic and diagrammatic in nature. As more param-

eters are resolved and relationships between variables quantified, the researcher revises models to make them more robust. A good example of this process is the progression of the parameterization of the models and the adaptive revisions made during a study of the occupancy of threatened lizards, and the reptile communities in general, in xeric sand dune habitats in southern California in order to understand habitats and their physical response to anthropogenic land use changes (Barrows, 1996; Griffiths et al., 2002; Barrows and Allen, 2010). The result was a more robust study design and better management options. Studies often are designed to test some future action, such as the changes in a riverine system after a dam is constructed upstream or predictions of responses from climate change. Conceptual models can be developed for future scenarios based on the litera- ture and knowledge from comparative systems, and the uncertainties in adapting these to the current situation can be described. When sampling is punctuated in time, espe- cially involving different observers over time, appropriate methods and observer bias must be clearly understood. Sampling variability can be part of the conceptual model,

as any sources of data collection bias should inform the uncertainty of the results of the study. There are good examples of robust studies in which sampling intervals are long and others in which they are short. Sampling methods and placement of sampling sites must be well documented to limit ambiguity when sampling repeatedly over time (see Chapter 3).

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| Planning and setting objectives in field studies

2.5 Sampling considerations

Tools that can be used to enhance sampling include digital databases of vouchered specimens and geospatial covariate climate data. An example from the Global Biodiversity Information Facility (GBIF; gbif.org) illustrates the contrast in density of specimen records (all taxa, not just reptiles) or observations from western Europe versus northern Africa (Figure 2.1). Such data can be used either to locate global or local gaps in biodiversity sampling or to provide a historic framework for a study. An illustration of this is the change in composi- tion of observations or records for reptiles and amphibians from southern California over the last 20 years. A graph of specimens archived in museums per year over the last 170 years shows some peaks where large numbers were accumulated one year or several years in sequence, and large gaps where few or no specimens were registered (Figure 2.2). In the last 20 years, almost all recent records used for modelling and identifying trends resulted from a large pit-fall trap study; very few specimens were archived in museum collections because the majority of animals were released alive after capture (Franklin et al., 2009; Figure 2.2). This means that future researchers will have to accept the accuracy of field pit-fall trap iden- tifications when comparing datasets, whereas they can verify the identification of archived specimens. Future datasets of species distributions (presence only, typically) will increas- ingly be composed of records from citizen scientists and in-field voucher photos, assuming accurate identification. An example of such a robust online database is the Herpetological Education & Research Project (http://www.naherp.com/), which currently has 2840 con- tributors and more than 220,000 records of reptiles and amphibians (August 2015). Another useful resource is The Reptile Database (http://www.reptile-database.org/; Uetz, 2014), which provides an up-to-date list of all currently recognized reptile species. This is a great resource of information and it illustrates well how fast our knowledge of the diversity of reptiles is increasing. For instance, when I finished my postdoctoral

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Figure 2.1 Distribution of 466,839,088 georeferenced global occurrence records from GBIF (gbif.org) covering all taxa. White and grey shading/stippling represent individual record locations. Dark areas lack any records for any species in the GBIF database. The contrast in records from western Europe (A) to northern Africa (B) is very striking and illustrates the biodiversity knowledge inequality between these regions. Someone asking a research question in western Europe would have much baseline data available to think through in study design, whereas someone in northern Africa might not.

Sampling considerations | 21

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Figure 2.2 Museum records (black bars) for five southern California counties for the last 170 years (N = 90,918) showing clear peaks in vouchers collected. On the right side of the graph are records from the U.S. Geological Survey pitfall trap sites (grey bars) from these same five counties from 1995 to present (N = 91,541). The majority of the later samples were field collected and released, illustrating the shifting types of data available for discerning future trends and comparing distributions.

research in 1998, 8000 species of reptiles were known; currently more than 10,000 species are known, a 20% increase in less than 20 years. Using up-to-date taxonomy is critical to prevent future confusion in the literature regarding which species were studied. Moreover, many researchers fail to publish geospatial coordinates for sampling locations or report them at a coarse resolution, making it difficult to determine which species was collected, especially when species complexes are sampled and vouchers are not saved. This is extremely important as over time, many taxonomic changes will be made. Changes in species lists for a particular location over time may be more indicative of name changes than of changes in occurrence. Species names can also be tracked through the Integrated Taxonomic Information System (ITIS; www.itis.gov; Hardisty et al., 2013). This system assigns a taxonomic ser- ial number (TSN) to each named entity such that it has a unique identifier that allows changes in taxonomy to be tracked; the TSN can be stored as a value in the database with the species names. There are currently (30 April 2015) 684,369 scientific names (not just species, but across all taxonomic ranks) with TSNs. The value of this system can be illustrated by a large standardized inventory/ monitoring programme carried out across coastal and desert transitional southern California habitats. When I started this programme in 1995, I developed a list of 49 reptile species that I might expect to detect within this geographic area (Table 2.2).