405_zacatuche_F-CN

THERYA, 2016, Vol. 7 (2): 333-342 DOI: 10.12933/therya-16-405, ISSN 2007-3364

Distribución y densidad del conejo zacatuche (Romerolagus diazi)

en el Área Natural Protegida Corredor Biológico Chichinautzin

Distribution and density of the zacatuche rabbit (Romerolagus diazi) at the Protected Natural Area "Corredor Biológico Chichinautzin"

Areli Rizo-Aguilar1, Christian Delfín-Alfonso2, Alberto González-Romero3 y José Antonio Guerrero1*

1 Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos. Av. Universidad 1001, 62209. Cuernavaca, Morelos, México. Email: areli.rizo@uaem.mx (ARA), aguerrero@uaem.mx (JAG).

2 Instituto de Investigaciones Biológicas, Universidad Veracruzana. Av. Luis Castelazo Ayala s/n, 91190. Xalapa, Veracruz, México Email: cada7305@gmail.com (CDA).

3 Instituto de Ecología, A. C. Carretera antigüa a Coatepec N° 351, El Haya, 91070. Xalapa, Veracruz, México. Email: alberto.gonzalez@inecol.mx (AGR).

*Corresponding author

The Protected Natural Area (PNA) “Corredor Biológico Chichinautzin” contains a large area of bunchgrasses, a habitat that is necessary for the zacatuche rabbit to survive. As part of a monitoring program used to evaluate the status of the zacatuche rabbit’s populations within this PNA, we estimated its distribution by using direct (sightings) and indirect methods (latrines) during visits performed to all the available habitats. Additionally, we estimated the annual density of the zacatuche rabbit using a line transect method, sampling eight, one-kilometer-long transects monthly during one year. Based on 101 latrine records and 48 sightings, a distribution map was prepared for the region using the convex polygon method in ArcView. Most of this distribution (166.43 km2) represents an area that had not been previously reported in the literature for the zacatuche rabbit. Using the half-normal model that best fit the data, we estimated a density of 4.2 rabbits/ha. Our results suggest that the Corredor Biológico Chichinautzin meets the criteria necessary to be cataloged as a core distribution area for the zacatuche rabbit. Therefore, we suggest that both management and conservation of this habitat within the PNA should be made a priority.

El Área Natural Protegida (ANP) “Corredor Biológico Chichinautzin” contiene una extensa área de pastizales amacollados, un hábitat que es necesario para que el zacatuche sobreviva. Como parte de un programa de monitoreo para evaluar el estado de las poblaciones del conejo zacatuche en esta ANP, estimamos su distribución utilizando métodos directos (avistamientos) e indirectos (letrinas) durante visitas a todos los hábitats disponibles. Además, se estimó su densidad anual utilizando el método de transectos lineales, muestreando cada mes ocho transectos de un km de largo durante un año. Con base en los registros de 101 letrinas y 48 avistamientos, se elaboró un mapa de distribución para la región mediante el método del polígono convexo en ArcView. La mayor parte de esta distribución (166,43 km2) representa un área que no habían sido previamente reportada en la literatura para el zacatuche. Usando el modelo half-normal que fue el mejor que se ajustó a los datos, se estimó una densidad de 4.2 conejos/ha. Nuestros resultados sugieren que el Corredor Biológico Chichinautzin cumple con los criterios necesarios para ser catalogado como un área núcleo de distribución para el zacatuche. Por lo tanto, sugerimos que el manejo y la conservación de este hábitat en el ANP deben ser una prioridad.

Key words: conservation, density, distribution, IUCN Romerolagus diazi.

© 2016 Asociación Mexicana de Mastozoología, www.mastozoologiamexicana.org

Introduction

The zacatuche rabbit (Romerolagus diazi) is an endemic species to the Trans-Mexican Volcanic Belt. Previous studies have indicated that the zacatuche rabbit has a strong preference for subalpine habitats (2,800-4,200 m), with higher abundances found in open pine forests (Pinus spp.) that have abundant bunch grasses (Festuca tolucensis, Muhlenbergia spp., Jarava ichu) in their understory (Velázquez and Heil 1996; Rizo-Aguilar et al. 2015). Based on this, the zacatuche rabbit is considered a habitat specialist. Its habitat has been severely fragmented due to factors such as urbanization, agricultural conversion, illegal logging, and wildfires (Velázquez et al. 2011). As a result, the species is classified as endangered on the IUCN Red List (AMCELA et al. 2008), and as at risk of extinction by Mexican Legislation (SEMARNAT 2010).

Until the late 1980s the precise area of distribution of R. diazi was unknown. López-Forment and Cervantes (1979) estimated that its area covered a total of 150 km2. In contrast, Hoth et al. (1987) only found zacatuche rabbits in three isolated areas in the central Trans-Mexican Volcanic Belt: the Sierra Nevada mountains, and the Tlaloc and Pelado volcanoes. The total area of distribution estimated by Hoth et al. (1987) was 280 km2. Motivated by these contrasting findings, Velázquez et al. (1996) conducted a survey throughout the proposed geographic range of R. diazi to document its historical and current distribution. Based on collection records, sightings, traces (pellets) and interviews with farmers, they estimated a distribution area of 386 km2. Within this, four core and 12 peripheral areas were recognized. This information was used to do the distributions maps for the zacatuche rabbit that are now available in the literature and on web pages (Velázquez et al. 1996; AMCELA et al. 2008).

Studies conducted on the Pelado Volcano, one of the four core areas of zacatuche rabbit, indicated that densities estimated using line transects ranged from 0.11 to 1.20 rabbits/ha according to habitat characteristics (Velázquez 1994). Other studies conducted on the Pelado, Tláloc and Iztaccíhuatl Volcanoes based on fecal pellet counts have shown that the abundance of this species is highly variable, ranging from 0.1 to 3.1 latrines/m2 (Velázquez 1994; Velázquez and Heil 1996; Velázquez et al. 1996).

The Corredor Biológico Chichinautzin (hereafter COBIOCH) is a Protected Area located in the northern part of the state of Morelos (Figure 1). The area of the COBIOCH (657.2 km2) includes Fractions I and II, covering the zone between Lagunas de Zempoala and El Tepozteco National Parks, and creating a biological corridor that ensures the continuity of ecological processes of the biota in the area. It contains on of the largest areas of grassland in centra Mexico (Cabrera-García et al. 2006), and likely acts as a corridor connecting the zacatuche rabbit populations of two core areas of its distribution, the Tláloc Volcano with those of the Pelado Volcano (Velázquez et al. 1996). Paradoxically, very little is known about the current status of Romerolagus diazi in the area, and there are only a few historical records dating from Velázquez et al. (1996).

In this paper we provide evidence of newly occupied areas by R. diazi as well as its annual density within the COBIOCH and its influence area. The outcomes are further discussed in the light of the relevance of this protected area for conservation of the endangered zacatuche rabbit.

Material and Methods

To document the distribution of the zacatuche rabbit, from June to November 2008, and from June to December 2011 we randomly selected 173 points (Appendix 1) from all habitats with bunchgrasses in the COBIOCH. Each point consisted of an area of 50 x 50 m within which exhaustive searches were conducted and latrines counted by at least 4 people. The zacatuche faeces are reliably distinguished from the ones of the other two lagomorphs Sylvilagus floridanus and S. cunicularius due to their size and shape (Hoth et al. 1987). The latrine counting method has been used previously to document the abundance and distribution of the zacatuche rabbit (Fa et al. 1992; Velázquez 1994). In addition, we recorded all zacatuches sighted along the roads and in the grasslands while driving or walking between sampling sites. Each sampling point and rabbit sighting was recorded using the Universal Transverse Mercator (UTM) geographic coordinate system, and was uploaded to a Geographical Positioning System software using a Garmin GPS device (coordinate output to WGS84). With these records, we estimated the area of distribution for the species within the COBIOCH, and we compared it to the distribution area estimated using all of the records reported by Velázquez et al. (1996). In both cases, we first generated a buffer area of 100 m in radius around the location of each record, to determine the area where the species might be located. We then estimated its probable distribution area using the Minimum Convex Polygon method, and the Fixed Kernel Isopleths method, both at a 95 % confidence level (Harris et al. 1990; Worton 1995). The output models for each method were combined spatially (MCP + Kernel model), and were subsequently cut with contours above 2,800 m, the lower elevation limit recorded for the area; finally we intersected it with the polygon of the COBIOCH to measure the area that lies within the protected natural area. The process was performed using the “Animal Movement Analyst” for ArcView 3.2.

The annual density of the zacatuche rabbit was estimated using the line transect method (Buckland et al. 1993). For this, eight reasonably straight, permanent 1000-m-long walking line transects were established, at least 1 km apart, to cover different habitats. Monthly zacatuche rabbit surveys were conducted from March 2010 to February 2011. Two experienced observers conducted the survey, both searching ahead and to each side of the transect while walking at a relatively constant speed of 0.5 km/h. All surveys were conducted between 7:00 and 9:00 h, which is the time of the day when the zacatuche rabbit is most active (Solorio-Damián 2013). The position of rabbits observed on the center line of the transect was recorded as a distance of zero, and for those observed to either side of the transect the distance (m) was recorded perpendicularly from the rabbit to the center line (Buckland et al. 1993) using an electronic distance measuring tool, the Multi Measure Combo Pro (Sonin Inc.). The data were analyzed using the Distance 5.0 program (Thomas et al. 2010) to estimate rabbit density per hectare. To model the detection function of the perpendicular distances, data were pooled across all transects. Three models were considered for the detection function: half-normal, uniform and hazard rate. In each case, the need for cosine adjustment terms was assessed using likelihood ratio tests. In all analyses, 5 % of the longest distances were shortened to avoid bias introduced by outlier distance sightings. The final model was chosen based on a combination of a low value for Akaike’s information criterion (AIC) and low variance.

Results

The presence of the zacatuche rabbit was documented at 149 points within the northernmost part of the COBIOCH. It was absent from 24 points with suitable habitat. The records include 48 sightings and 101 pellet counts. The estimated occupied area based on 49 historical records was 56.85 ha. Based on all our field records, the estimated area occupied by this species in the Protected Natural Area and the zone of influence was 166.43 km2 (Table 1). Most of this estimated area (98 ha) is located within the polygon of the COBIOCH. Comparing this area with that estimated based on historical records (Figure 2), this one represents an increase of 109 ha of the occupied area previously known.

During the 12 months of the density survey, a total of 97 zacatuche rabbits were sighted along 96 km of transect. The analysis of this data using the Distance 5.0 software indicates that the half-normal + 1cosine model provided the best fit to our distance data according to the AIC and variance values (Table 2). This model estimates a density of 4.2 individuals/ha.

Discussion

Our results represent an increase of the knowledge related to the range of the distribution for R. diazi into the COBIOCH and its influence zone. Most of the recent estimated area was not included in the distribution map proposed by Velázquez et al. (1996), which is the basis for the IUCN map (IUCN 2012). Clearly, our findings do not represent an expansion of the zacatuche rabbit in the Sierra de Chihinautzin, but reflects our intensive sampling. Before our field survey, there were only 49 historical records based on collecting data, literature and field surveys conducted in the study area (Appendixes 2 and 3 in Velázquez et al. 1996).

Velázquez et al. (1996) based on those records, together with an analysis of climate, elevation and vegetation maps along the Trans-Mexican Volcanic Belt, recognized six peripheral areas (isolated from each other) for the zacatuche rabbit within the area inside the COBIOCH. Our direct and indirect records point to a different scenario. First, the proximity of all the records indicates that the populations of the zacatuche rabbit might not be isolated from each other and that the rabbits are likely moving between landscapes. The only barrier to dispersal is the highway 95D (Mexico City-Cuernavaca), built in 1952, that crosses the COBIOCH and has barred connectivity between populations on either side of it (Uriostegui-Velarde 2014). Second, Velázquez et al. (1996) recognized as core distribution areas of R. diazi those with suitable habitat where rabbits were sighted and traces (pellets) were found. The results presented here clearly meet these criteria, therefore indicating that the COBIOCH must be also considered a core area of the zacatuche rabbit. Added to that, our result regarding the estimated annual density also provides evidence that the COBIOCH is one of the most important habitats for zacatuche rabbit populations. Density estimated is higher than the only previous report of 1.2 rabbits/ha for the area of the Pelado Volcano using a similar methodology (Velázquez 1994).

These results make an important contribution to our knowledge of the distribution of R. diazi, and the evidence regarding its occurrence and density obtained during this study allow us to suggest that the COBIOCH provides a suitable habitat with conditions that are appropriate for R. diazi to establish and maintain populations with high abundances. It is therefore necessary to implement conservation actions that focus on habitat management and protection in order to avoid the habitat loss and fragmentation that result from grazing, crop cultivation and road construction.

Acknowledgements

We thank all students of the Facultad de Ciencias Biológicas, of the Universidad Autónoma del Estado de Morelos for helping with the field-work. This study was partially funded by the Comisión Nacional de Áreas Naturales Protegidas. A. Rizo-Aguilar received a graduate studies scholarship from CONACYT (44564).

Literature cited

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Submited: March 16, 2016

Reviewed: April 4, 2016

Accepted: April 26, 2016

Associated editor: Consuelo Lorenzo

Appendix 1

List of sampled points used to document both distribution and estimated occupied area of Romerolagus diazi within the COBIOCH.

X

Y

X

Y

1

481452.8630

2110266.7704

43

468505.3013

2110784.7857

2

478781.8766

2108370.8834

44

469682.3159

2110006.8160

3

479526.7436

2110152.6332

45

470225.3242

2107237.9499

4

478861.7115

2110455.5028

46

470238.8004

2107681.3369

5

477642.8210

2110156.6659

47

471039.5803

2107743.6436

6

469528.2843

2110561.6963

48

471139.3437

2107960.9222

7

470095.3161

2110646.8244

49

471508.5979

2111234.5920

8

470445.3828

2110280.5183

50

471635.9637

2111470.7897

9

478809.1557

2108203.6573

51

471849.9994

2106855.7496

10

478830.1949

2108710.7495

52

471862.5065

2107320.1455

11

478315.6355

2108526.9412

53

474542.1658

2112130.2452

12

478158.4247

2109034.2433

54

474630.8961

2112506.5556

13

478176.6789

2109642.7621

55

475018.2599

2112546.2835

14

478229.9038

2110171.3304

56

475210.9037

2112666.7673

15

479429.0815

2108525.6660

57

476852.6562

2111819.5911

16

479453.0189

2109026.6088

58

476968.6579

2111699.5974

17

477708.9807

2109529.6043

59

477487.0047

2110139.3884

18

477532.1418

2110694.6526

60

477742.3155

2110814.5933

19

477800.4594

2110267.1193

61

477865.0494

2109502.8715

20

479503.2318

2109506.0086

62

478043.0510

2110618.2535

21

478994.6300

2109395.9373

63

478257.6772

2109780.6970

22

479970.4083

2109148.9770

64

478317.6782

2108533.7618

23

480156.9184

2108666.2467

65

478590.6820

2111899.5868

24

480935.3395

2109691.9517

66

478613.6823

2111876.5880

25

481051.7239

2109200.0827

67

478635.6828

2109812.6953

26

481991.2748

2110720.4900

68

478876.6865

2108059.7864

27

482157.2441

2110111.7888

69

479007.7023

2110470.4311

28

481613.3426

2109734.2912

70

479029.6886

2110830.6423

29

474626.7103

2112185.9736

71

479262.6922

2108234.7773

30

473285.1538

2111895.8928

72

479355.0674

2110590.4048

31

473812.5856

2110887.0433

73

479590.6359

2110537.2276

32

474329.0247

2110336.1694

74

479623.9575

2110290.3604

33

471690.5902

2106706.9106

75

479627.6977

2108285.7746

34

472060.6061

2106318.7862

76

479803.1711

2110296.3301

35

470734.5925

2105250.0526

77

479907.4957

2109789.8364

36

471624.5502

2111464.7116

78

480668.2739

2111484.5282

37

471503.6491

2110564.6831

79

481182.3305

2111519.5964

38

471056.1302

2110288.7695

80

481344.1039

2111424.8213

39

471595.5202

2109881.6200

81

481642.5134

2111279.8588

40

470552.3788

2109576.5260

82

481763.5223

2109955.8276

41

470741.5907

2109112.1335

83

481840.9954

2109294.4620

42

468210.2981

2109305.8626

84

482431.2751

2110350.7271

85

489211.6459

2109112.8611

127

477925.6722

2110676.6504

86

489946.5818

2109552.4782

128

478683.6835

2110448.6622

87

489958.9280

2108696.6827

129

477981.6730

2110646.6520

88

491000.6754

2108824.8860

130

478590.6820

2111899.5868

89

491996.6992

2109227.8650

131

478717.6840

2109849.6934

90

493376.7787

2107431.9383

132

477864.6714

2109502.7115

91

494102.9175

2105834.8814

133

498337.9753

2107662.8062

92

495393.7917

2107876.0152

134

477619.0386

2110806.2887

93

496656.6384

2108011.2581

135

477807.7744

2110858.5430

94

497617.1916

2108209.6678

136

477893.2357

2110876.4591

95

498305.8069

2107862.9158

137

477949.4276

2110846.6226

96

499402.8221

2107334.9533

138

478331.1302

2110758.0942

97

500963.8503

2107296.9553

139

478543.6815

2109444.7144

98

478591.6820

2111908.5864

140

478590.6820

2111899.5868

99

477435.6649

2111628.6010

141

478613.1484

2110814.6882

100

478694.6838

2109045.7352

142

478644.3449

2110663.8930

101

479592.6970

2110086.6810

143

478651.4440

2110648.8798

102

478676.6834

2110463.6614

144

478662.7023

2109246.1197

103

479541.6962

2110249.6725

145

478714.5491

2109067.4050

104

481348.7230

2111413.6119

146

478945.4344

2110604.2671

105

479543.6963

2110378.6658

147

479032.0286

2110827.5345

106

480008.7032

2110326.6685

148

479438.9327

2110545.8951

107

480402.7091

2109869.6922

149

479477.7503

2110453.7519

108

480681.7132

2109896.6908

150

479493.0675

2110066.1261

109

480681.7132

2109896.6908

151

479494.0925

2110433.4790

110

481936.7318

2110365.6663

152

479509.5507

2110450.2851

111

481592.7267

2110038.6833

153

479509.5507

2110450.2851

112

479526.6960

2110233.6733

154

479511.8728

2110579.1824

113

490556.8599

2108475.7641

155

479511.8728

2110579.1824

114

490169.8541

2108600.7576

156

479511.8728

2110579.1824

115

478363.6787

2110557.6566

157

479560.5735

2110287.1816

116

478645.6829

2110614.6536

158

479565.3606

2110016.3086

117

479063.6891

2110627.6529

159

479976.7657

2110526.3381

118

478746.6845

2108867.7444

160

480370.6836

2110069.6868

119

479509.6958

2110253.6723

161

480650.0997

2110096.7964

120

479597.6971

2109815.6951

162

481311.1034

2111624.8109

121

479525.6960

2109865.6925

163

481311.1034

2111624.8109

122

477839.6709

2110658.6514

164

481311.1034

2111624.8109

123

477651.6681

2110605.6542

165

481315.8615

2111613.7235

124

478977.6879

2110403.6645

166

481315.8615

2111613.7235

125

479471.6952

2110345.6675

167

481560.3622

2110238.3500

126

479387.6939

2110390.6652

168

481768.9663

2110476.9945

169

481904.4453

2110565.8179

170

490137.5356

2108800.6563

171

490525.0064

2108675.4957

172

491000.6754

2108824.8840

173

497585.1912

2108408.6525

Figure 1. Location of the Corredor Biológico Chichinautzin Protected Area in Mexico. Lagunas de Zempoala National Park (LZNP).;Fraction I (FI) Fraction II (FII); El Tepozteco National Park (TNP).

Table 1. Estimated area occupied by Romerolagus diazi (km2) based on historical and recent records for the Corredor Biológico Chichinautzin (COBIOCH) Protected Natural Area.

Estimated area (km2)

Historical records

Recent records

Fractions I and II

32.09

98.96

El Tepozteco

8.64

46.88

Lagunas de Zempoala

16.12

20.59

Total area

56.85

166.43

Table 2. Annual density (D) of Romerolagus diazi estimated using Akaike’s information criterion (AIC) and the percent coefficient of variation (% CV) for each model.

Model

AIC

D

% CV

Half-normal + 1 cosine

614.24

4.2

10.1

Unifrom + 1 cosine

675.68

7.7

14.7

Hazard rate + 1 cosine

668.13

8.1

12.5

Figure 2. Distribution area of Romerolagus diazi within the Corredor Biológico Chichinautzin based on historical and recent records. LZNP, Lagunas de Zempoala National Park. FI, Fraction I. FII, Fraction II. TNP, El Tepozteco National Park. Estimated areas are provided in Table 1.

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FACTOR DE IMPACTO 2020 (SCOPUS): 1.2


THERYA es publicada por la Asociación Mexicana de Mastozoología A. C.  Se distribuye bajo una Licencia de Creative Commons Atribución-NoComercial-SinDerivar 4.0 Internacional.

DERECHOS DE AUTOR Y DERECHOS CONEXOS, THERYA es una publicación digital cuatrimestral editada por la Asociación Mexicana de Mastozoología A. C.  Hacienda Vista Hermosa 107, Colonia Villa Quietud, Coyoacan 04960.  Distrito Federal, México.  Telefono (612) 123-8486, www.mastozoologiamexicana.org.  Editor responsable: Dr. Sergio Ticul Álvarez Castañeda (therya@cibnor.mx).  Reservas de Derechos al Uso Exclusivo No. 04-2009-112812171700-102, ISSN: 2007-3364 ambos otorgados por el Instituto Nacional de Derechos de Autor.  Responsable de la última actualización de este número, Unidad de informática de la Asociación Mexicana de Mastozoología A. C.  Dr. Sergio Ticul Álvarez Castañeda.  Instituto Politécnico Nacional 195.  La Paz, Baja California Sur, C. P. 23096.  Tel 612 123 8486.