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Herpetofauna diversity in Kitobo forest, Kenya/Diversidad de herpetofauna en la Selva Kitobo, Kenia.

INTRODUCTION

Understanding species distribution is very crucial if the conservation of the species and their habitats is to be realized. Threats to biological resources are highest in the tropics where biodiversity is as well highest (Myers 2003). The need to conserve biodiversity is now more urgent than ever as unsustainable use of natural resources escalates.

The East African region presents very complex terrestrial ecological zones ranging from lowland coastal forest, deserts, dry woodland, grasslands to rainforest habitats. The diverse terrestrial habitats also support a very complex diversity of floral and faunal species many of which are endemic. In East Africa the need to understand herpetofaunal species distribution has been ongoing for years (see Loveridge 1957) and in different areas, e.g. tropical rainforest (Schick et al. 2005, Lotters et al. 2007, Wagner and Bohme 2007, Wagner et al. 2008); coastal forests (Drewes 1992, Chira 1993, Howell 1993, Malonza et al. 2006a); highland forests (Lotters et al. 2006); dryland areas (Malonza et al. 2006b, Wasonga et al. 2006) and Eastern Arc Mountains (Barbour and Loveridge 1928, Poynton 2003, Loader et al. 2004, Doggart et al. 2006, Burgess et al. 2007, Poynton et al. 2007, Menegon et al. 2008, Malonza 2008).

From the above studies it is evident that a lot has been done within the Eastern Arc Mountains and the coastal forests of Tanzania and Kenya, which are well-known world biodiversity hotpots (Myers et al. 2000, Mittermeier et al. 2004). However, species diversity in certain areas still remains largely unknown making their biogeographical affinity uncertain. One such area is the ground water Kitobo forest in southern Kenya. This is an island in a sea of arid lands and acts as species refugia. Therefore species composition in this forest could be very interesting due to edge effects from the surrounding arid matrix (Fagan et al. 1999, Urbina-Cardona et al. 2006). Whenever ecological aspects of edge have been studied, many have observed patterns of increased species richness at habitat edges (Fagan 1999). What is more important is to understand the links between habitat edge and community dynamics. To understand how the habitat edges affect the diversity of amphibians and reptiles, it is important to determine the changes in species composition along the gradient from the edge to the interior of the forest. Studies have shown that amphibians and reptiles found in the forest interior, which tend to avoid the edges, are more susceptible to extinction (Urbina-Cardona et al. 2006). Understanding the amphibian and reptile species response to microhabitat disturbance in arid land insuralized forest habitats is vital in designing their conservation strategies. In this study, we evaluated changes in amphibian and reptile diversity along the edge to interior forest. Species were grouped into assemblages based on their affinities for forest edge and forest interior habitats. We tested specific research questions such as: (1) is there any difference in species composition between habitats? (2) is there any difference in species richness between habitats?

MATERIALS AND METHODS

Study Area

The Kitobo Forest is a ground water forest located about 10 Km South-East of Taveta town in the Taita-Taveta district, Coast Province, Kenya (Fig. 1). It is approximately 250 km inland from the coast and on the extreme lowland North-East of the Tanzanian Eastern Arc Mountain block of North Pare Mountains near the Kenya-Tanzania border (UTM: 9619706, 346407; 9618900, 345790). It covers an area of ca. 160 ha at an altitude of about 750 m above sea level. It is largely an evergreen indigenous forest surrounded by arid lands of Acacia bushes. It owes its existence to the eruption on its edge of a large Njoro spring plus other small ones inside the forest originating from the volcanic Mt. Kilimanjaro. The springs then develop into a permanent stream that flow through the forest. Bordering the forest on the southern and eastern parts are irrigation schemes that utilize water from these springs and other water canals growing rice, onions, maize, bananas, tomatoes, mangoes and citrus (Fig. 2).

[FIGURE 1 OMITTED]

Definition of the sampling habitats

1) Forest edge

In this study the edge refers to the transition habitat between natural evergreen forest and the bush land habitat. This was an interface belt comprising bush and wetland habitats along the forest border.

2) Forest interior

This is the evergreen forest within which occur natural swamps, springs, streams and ponds.

Herpetofaunal sampling

Surveys were conducted on three occasions: from 7 to 11 December 2007, from 5 to 13 December 2009, and from 00 to 00 April 2010.

Methods used for recording amphibians and reptiles (day and night) included standardized time-limited searches and pitfall traps associated with drift fences.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Time limited searches (TLS) method as described by Karns (1986), Heyer et al. (1994), Sutherland (1996) was used. It was done within the forest edge and interior habitats for one person hour both day and night. During the searches all possible microhabitats such as under leaves, debris, decomposing tree stumps, on tree, shrubs, bushes and logs, including digging were intensively searched. Quantitative species data analysis used TLS data.

X-shaped drift fence with pitfall traps, a modification of that used by Corn (1994) with segments of 5 m length were used. The pitfall traps consisted of 10 l plastic buckets flush with the ground; in total, every trap array had Ave buckets. Two trap sets were established in the forest interior for Ave days in the first occasion and seven days in the second. Traps were used for detection of small primarily nocturnal crawling herpetofauna not easily detected through other methods.

Species richness and diversity analysis

Herpetofaunal species diversity was measured using the Shannon Index (H'). The observed species richness was estimated using the Estimates 7.5.1 program (Colwell, 2006). Jacknife 1 species richness estimator was compared with observed species richness (Sobs). Species accumulation curves were calculated and generated using the software programme EstimateS using 1000 randomizations (Fig. 3). The species richness was plotted as a function of the accumulated number of samples (time-limited-searches).

Identification of the specimens was made using published taxonomic keys (Spawls et al. 2002, Channing and Howell 2006) and taxonomy for amphibians followed by Frost et al. (2006) and Frost (2007). Selected individuals of underrepresented species were kept as voucher specimens and deposited in National Museums of Kenya (NMK).

Voucher specimens except amphibian larvae were fixed in 10 % formalin (after euthanasia). Tissues of selected specimens were preserved in absolute alcohol for the possibility of later molecular analyses. Tadpoles were fixed in 95% ethanol. All specimens collected are deposited at NMK. Colour photos of selected species and their habitats were taken. GPS data were determined using a 12 Channel Garmin[R] receiver.

Statistical analyses

Two sample t-tests (independent samples) were used to compare species abundance and species richness between forest edge and forest interior. Data was analyzed with STATISTICA 6.0 software (StatSoft, 2001) at 5% significance level.

RESULTS

Species diversity and composition patterns

After 37 time-limited searches (TLS) at the forest edge, 180 individuals of 10 amphibian species and 104 individuals of 22 reptile species were recorded. After 46 TLS samples in the forest interior, 165 individuals of nine amphibian species and 132 individuals of 16 reptile species were recorded. After 12 days of trapping, six species (five amphibians, one reptile) were captured with the amphibians Hemisus marmoratus (Peters, 1854) being the most abundant. More important was that it was only through traps that the aquatic frog Xenopus muelleri (Peters, 1844) was detected (Table 1).

The species diversity per sampling effort (TLS) was significantly higher in the forest edge than in the forest interior (t-test independent samples: Amphibians; t = 3.37, df = 81, [n.sub.1] = 37, [n.sub.2] = 46, P = 0.001: Reptiles; t = 6.65, P < 0.001). However, the number of species detected per TLS sample was not significantly different between the two habitats (Amphibians; t = 0.146, df = 81, [n.sub.1] = 37, [n.sub.2] = 46, P = 0.88: Reptiles; t = -0.166, P=0.87). Again, the number of individuals per species detected was also not significantly different between forest edge and forest interior (Amphibians; t = -0.047, df = 17, [n.sub.1] = 10, [n.sub.2] = 9, P = 0.96: Reptiles; t = 1.72, df = 136, [n.sub.1] = 22, [n.sub.2] = 16, P = 0.088). Both the forest interior and forest edge were dominated by the lizard Trachylepis maculilabris (Gray, 1845) while for amphibians the forest interior was dominated by the frog Phrynobatrachus acridoides (Cope, 1867) and the reed frog Hyperolius glandicolor (Peters, 1879), in the forest edge aquatic swamps. At night on the forest edge, the Flap-necked Chameleon Chamaeleo dilepis Leach, 1819 was the most dominant (Table 1).

From species accumulation curves, the number of reptile species observed in both the forest edge and forest interior increased with increasing sampling effort. Amphibian species observed seemed to plateau with additional sampling, especially on the forest edge (Fig. 3). The species richness estimator, Jacknife 1, was in many cases always higher than observed species (Sobs).

The Bibron's burrowing asp Atractaspis bibronii A. Smith, 1849, was detected through opportunistic visual encounter survey inside the forest. The local people reported the presence of spectacular large snakes like Puff-Adder Bitis arietans (Merrem, 1820), Southern African rock python (Python natalensis A. Smith, 1840), Black-necked spitting cobra (Naja nigricollis Reinhardt, 1843) and Dendroaspis polylepis (Gunther, 1864).

Discussion

Our results demonstrate that the number of species and the total number of individuals per species was not different at forest edge and forest interior. This is attributable to the fact that the forest edge and the forest interior had almost similar micro-habitats. Therefore most of the species detected at the forest edges came from inside the forest for thermoregulation (Zug 2001). However, the species diversity per sample was significantly higher at the forest edge habitat. This concurs with the well known phenomenon of edge effects (Fagan 1999).

In general, the species accumulation curves did not reach an asymptote, indicating that more species could be detected with additional sampling. This is particularly so for reptiles due to the influx of species from the surrounding arid lands using the evergreen forest as refuge.

The forest edge was expected to harbour more species of amphibians that breed on open water due to the presence of diverse wetlands. However, our results demonstrated that the forest edge matrix was not necessarily an ideal habitat for the reproduction and maintenance of all amphibians. This could be due to the continuous disturbance of these micro-habitats by farmers, e.g. on the rice fields. Notable was the tree frog, Leptopelis flavomaculatus, which avoided habitats outside the evergreen forest. Therefore it is clear that the evergreen forest is a refuge for all the species that occur on the forest edge and the surrounding matrix and more so during the dry season.

Biogeographically, the presence of species such as Leptopelis flavomaculatus, Hyperolius puncticulatus (Pfeffer, 1893) and Thelotornis mossambicanus (Bocage, 1895) that are present in the typical coastal forest of Arabuko-Sokoke provide an evidence that Kitobo forest species has close affinities with coastal forests (Drewes 1992, Chira 1993, Howell 1993, Schi0tz 1999, Spawls et al. 2002, Channing and Howell 2006, Burgess et al. 2007). All these species are also present in the coastal forests of Shimba Hills but this also shares a lot with the Eastern Arc Mountains, especially East Usambara Mountains of Tanzania (Howell 1993, Spawls et al. 2002, Malonza and Measey 2005, Channing and Howell 2006).

Despite its long distant from the coast, the herpetofaunal composition of Kitobo forest demonstrates that there are historical relationships among its fauna with the coastal forests. This therefore reflects shared environmental factors (temperature, humidity and salinity) that resulted to its colonization by similar fauna, as suggested by current ecological biogeography theory (e.g. Monge-Najera 2008).

Conservation implications

Forest associated species such the tree frog Leptopelis flavomaculatus and Hyperolius puncticulatus (Pfeffer, 1893) in our results are of conservation concern. These species reflect the habitat quality of the forest interior and their disappearance may be an indication of habitat degradation within this "island" forest refuge. Such species should be monitored more closely, since they are highly sensitive to habitat disturbance and are often the most vulnerable to habitat modification. Such species easily disappear from forest fragments after isolation and can even suffer local extinction (Urbina-Cardona et al. 2006). All efforts should be made to conserve the arid land paradise as a biodiversity important area with high potential for establishment of community-based ecotourism projects for sustainable community livelihood development.

ACKNOWLEDGMENTS

We wish to thank Joash Nyamache, our NMK field technologist, for his help in preservation, and Johana Mwawasi Nusu, the Kenya Forest Service guard, for his assistance and good knowledge of the forest. This survey was funded by the National Museums of Kenya, Nairobi and the Mohamed Bin Zayed (MBZ) Species Conservation Fund.

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PATRICK K. MALONZA (1,2) and BERYL A. BWONG (1)

(1) Section of Herpetology, National Museums of Kenya P. O. Box 40658-00100, Nairobi, Kenya

(2) Send correspondence to / Enviar correspondencia a: kmalonza@museums.or.ke
TABLE 1. Species distribution and number of individuals detected
using time-limited searches (46 at the forest interior and 37 at the
forest edge). Abundance of those also caught during the 12 trapping
days are indicated within parentheses

TABLA 1. Distribucion de especies y numero de individuos detectados a
traves de busquedas con tiempo restringido (46 en el interior de la
selva, 37 en el borde de selva) La abundancia de aquellas capturadas
durante los 12 dias de trampeo se indica dentro de parentesis.

SPECIES Forest Forest
 edge interior

AMPHIBIANS

Pipidae
Xenopus cf. muelleri (Peters, 1844) -- (2)

Bufonidae
Amietophrynus gutturalis (Power, 1927) 9 3
Amietophrynus steindachneri (Pfeffer, 1893) 10 5
Amietophrynus xeros (Tandy, Keith et 3 --
 Duff-Mackay, 1976)

Hemisotidae
Hemisus marmoratus (Peters, 1854) 9 1

Arthroleptidae
Leptopelis flavomaculatus (Gunther, 1864) -- 27

Hyeproliidae
Hyperolius glandicolor (Peters, 1879) 55 28
Hyperolius cf. puncticulatus (Pfeffer, 1893) 12 25
Hyperolius tuberilinguis Smith, 1849 22 --

Ptychadinidae
Ptychadena anchietae (Bocage, 1867) 14 2
Ptychadena mascareniensis (Dumeril et 27 29
 Bibron, 1841)

Phrynobatrachidae
Phrynobatrachus cf. acridoides (Cope, 1867) 19 45

REPTILES

Lizards
Gekkonidae
Lygodactylus sp. 1 --
Lygodactylus luteopicturatus Pasteur, 1964 17 1
Hemidactylus platycephalus Peters, 1854 3 11
Hemidactylus mabouia (Moreau de Jonnes, 1818) 12 6
Hemidactylus squamulatus Tornier, 1896 1 --
Cnemaspis cf. africana (Werner, 1895) -- 1

Chamaeleonidae
Chamaeleo dilepis Leach, 1819 16 --

Scincidae
Melanoseps loveridgei Brygoo et Roux-Esteve, -- 14
 1981
Lygosoma sundevalli (A. Smith, 1849) 1 5
Panaspis cf. wahlbergii (A. Smith, 1849) 1 --
Trachylepis maculilabris (Gray, 1845) 27 47
Trachylepis striata (Peters, 1854) 15 4
Trachylepis planifrons (Peters, 1878) 1 --
Trachylepis brevicollis (Weigmann, 1837) 5 --

Lacertidae
Latastia longicaudata (Reuss, 1834) 5 --

Agamidae
Agama lionotus Boulenger, 1896 6 --

Gerrhosauridae
Gerrhosaurus major Dumeril, 1851 2 --
Gerrhosaurus flavigularis Wiegmann, 1828 4 --

Varanidae
Varanus niloticus (Linnaeus, 1766) 1 5
Varanus albigularis (Daudin, 1802) 2 --

Snakes
Leptotyphlopidae

Leptotyphlops scutifrons merkeri (Werner, 1909) 1 1

Pythonidae
* Python natalensis A. Smith, 1840 -- --

Colubridae
Lycophidion capense (A. Smith, 1831) -- 1
Philothamnus battersbyi Loveridge, 1951 7 2
Philothamnus punctatus Peters, 1866 -- 1
Thelotornis mossambicanus (Bocage, 1895) 1 --
Dasypeltis medici medici (Bianconi, 1859) -- 2
Prosymna stuhlmanni (Pfeffer, 1893) 1 --

Atractaspididae
** Atractaspis bibronii A. Smith, 1849 -- 1

Elapidae
* Naja nigricollis Reinhardt, 1843
Dendroaspis angusticeps (A. Smith, 1849) -- 1

* Dendroaspis polylepis (Gunther, 1864)

Viperidae
* Bitis arietans (Merrem, 1820) -- --

Crocodiles
Crocodylidae
* Crocodylus niloticus Laurenti, 1768 -- --

Note: * Species reported to be present by the local people but not
recorded during this survey. ** Species detected through
opportunistic survey.

Nota: * Especies reportadas por gente local de estar presentes pero
que no fueron registradas durante los muestreos. ** Especies
detectadas a traves de muestreo casual.
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Author:Malonza, Patrick K.; Bwong, Beryl A.
Publication:Herpetotropicos: Tropical Amphibians & Reptiles
Date:Jan 1, 2010
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