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«A thesis submitted in partial fulfilment of the requirements for the degree of Magister Scientiae in the Department of Biodiversity and Conservation ...»

-- [ Page 1 ] --

The invasive guttural toad, Amietophrynus gutturalis

 

Nicolas S. Telford

 

 

 

A thesis submitted in partial fulfilment of the requirements for the degree of Magister

Scientiae in the Department of Biodiversity and Conservation Biology, University of the

Western Cape.

Funding provided by the National Research Foundation (NRF)

Ethics clearance

Ethics clearance for this project was granted by the UWC Ethics Committee 11 September

2013, ref 04/4/10

 

 

 

 

‘They have a predilection for macadamised roads at night and thus are squashed by passing motorists. On a 2 km long road that I traverse there may be 20 to 30 dead toads most mornings for months on end – the supply seems limitless – they must die in this way throughout the country in countless thousands.’ Wager, 1986 1

DECLARATION

    I declare that, The invasive guttural toad, Amietophrynus gutturalis, is my own work, that it has not been submitted for any degree or examination in any other university, and that all   the sources I have used or quoted have been indicated and acknowledged by complete   references.

Full name: Nicolas Simon Telford

Date:

Signed:

2

ABSTRACT

The invasive guttural toad, Amietophrynus gutturalis   N. S. Telford   MSc Thesis, Department of Biodiversity and Conservation Biology, University of the   Western Cape   The guttural toad, Amietophrynus gutturalis, Power 1927, is a common toad with a broad geographic range through much of temperate, sub-tropical and tropical southern and central Africa. Introduced to the islands of Mauritius and Reunion in the 1960’s, and subsequently to Cape Town in the 1990’s, the species has become invasive in its extra-limital ranges.

Determining the invasion history of a species provides valuable information for conservation biologists and managers and it is fundamentally important for improving our understanding of the underlying processes of biological invasions. This study aimed to determine the source populations of the extra-limital populations from Mauritius and Cape Town. Furthermore, studies investigating genetic diversity and demographics of African Bufonidae are largely absent from the literature. Understanding the evolutionary history of the species may also assist with determining their invasive ability and identifying similar features in other bufonids such as Amietophrynus regularis and A. xeros. Using mtDNA sequence data from the 16S and ND2 markers four geographically distinct clades were identified through Bayesian phylogenies and haplotype networks. However, a spatial analysis of molecular variance (SAMOVA) indicated a grouping structure of three clades. A total of 16 haplotypes were identified from 53 samples for the 16S marker and 22 haplotypes were identified from 43 samples for the ND2 marker. Both the Mauritius and Cape Town invasive populations were found to have originated from the eastern clade. However, they matched the common haplotype from this region which was found across a vast area that spans the KwaZulu-Natal province and into the Mpumulanga and Limpopo provinces. This did not allow for identifying a more precise region for the origin of the founder populations. The presence of haplotypes unique to the Cape Town invasive population, which group with the eastern clade, indicates that there has potentially been more than one introduction event. Demographic analysis revealed a recent population expansion in both the northern (Fs = -2.92) and the eastern clades (Fs = -5.03). Significant genetic variation was found among groups (93.92%), with low variation among populations and among populations within groups. Population pairwise differences were found to be significantly different between all clades except between the central and the southern clade. There was a negligible difference in the genetic

–  –  –

My sincere gratitude must be conveyed firstly to my supervisors Dr Vanessa Couldridge and Professor Alan Channing for their invaluable guidance, assistance, insight, funding assistance, provision of tissue samples and patience through the course of this project.

Without their assistance this project would never have come to fruition. I would also like to thank Professor John Measey from the Centre for Invasion Biology at Stellenbosch University, for providing the opportunity to use his research topic, for providing tissues from his own collection and the tissues from the toads collected from the Cape Town invasive population as well as for his assistance and guidance on various topics of the project. I would also like to thank Professor Krystal Tolley from the South African National Biodiversity Institute for assisting me with various aspects surrounding my biogeographical analysis and Dr Claudia Bader and Dr Vincent Florens from the University of Mauritius for providing invaluable samples from the invasive population of Mauritius. I would also like to thank Atherton de Villiers for valuable information provided regarding the invasive toad population in Cape Town.

Furthermore, the study would not have been possible without the bursary monies I received from the National Research Foundation and the University of the Western Cape, of which I am deeply grateful. I would also like to thank the Ezemvelo KZN Wildlife, Cape Nature, Eastern Cape Department of Environmental Affairs, and the Gauteng Directorate of Nature Conservation for the provision of permits and I am deeply grateful to all the private land owners that allowed me to collect samples on their land.





Last, but not least, I would like to express my deepest thanks to my family and close friends for their help, love and guidance over the duration of this study.

–  –  –

  DECLARATION

 

Abstract

  ACKNOWLEDGEMENTS

TABLE OF CONTENTS

LIST OF TABLES AND FIGURES

AIMS AND OBJECTIVES

CHAPTER 1

GENERAL INTRODUCTION

Background on Amietophrynus gutturalis

Hybridisation

Invasion history

Amphibian conservation and the threat of invasive species

Invasive amphibians of the Western Cape

Effects of invasive species on evolution

Background on toad biogeography

Reasoning behind study

CHAPTER 2

MATERIALS AND METHODS

Sampling

PCR amplification

DNA sequencing and alignment

Phylogenetics

Genetic diversity

Population genetic analyses

Demographics

CHAPTER 3

RESULTS

Phylogenetics

Haplotype networks

Genetic diversity of invasive populations

6 Population genetics of Amietophrynus gutturalis

Demographics

  CHAPTER 4

  DISCUSSION

  Population genetics

Demographics and biogeography

  Invasive Amietophrynus gutturalis

Where did the invasive populations originate from?

Genetic diversity

Biotic implications

Implications for conservation management

Recommendations for further research

REFERENCES

–  –  –

Table 3.1: Haplotype list for the 16S rRNA genetic marker showing the localities, clade and number of samples from each locality for each haplotype.

Haplotypes are numbered according to those represented in the haplotype network (Fig. 3.3).

Table 3.2: Haplotype list for the ND2 mtDNA genetic marker showing the localities, clade and number of samples from each locality for each haplotype.

Haplotypes are numbered according to those represented in the haplotype network (Fig. 3.4).

Table 3.3: Standard measures of genetic diversity of the source population compared to the Cape Town and Mauritius invasive populations of Amietophrynus gutturalis.

Sample size (n), nucleotide diversity (π) and haplotype diversity (h) shown with 95% confidence intervals (CI) in brackets.

Table 3.4: Results from the analysis of molecular variance (AMOVA) showing the percentage of variation among groups, among populations within groups and within populations as well as the associated F-statistics.

Table 3.5: Population pairwise ΦST values for the four geographic groups defined by SAMOVA.

Significant ΦST values (p 0.05) indicated by a * and highlighted in bold.

Table 3.6: Standard genetic diversity indices and neutrality tests for the four geographical regions indicated by the phylogenetic analysis of Amietophrynus gutturalis.

Sample size (n), nucleotide diversity (π) and haplotype diversity (h) shown with 95% confidence intervals (CI) in brackets. Fu’s Fs (Fs) test for selective neutrality shown with probability values (significant when P0.02; significant values highlighted in bold) in brackets.

–  –  –

Figure 3.1: Metropolis Coupled MCMC Bayesian inference phylogeny of Amietophrynus gutturalis derived from the 16S rRNA marker.

Maximum Likelihood bootstrap values greater than 70% are shown above and Bayesian posterior probabilities greater than 0.7 are shown below branches at terminal nodes.

Figure 3.2: Metropolis Coupled MCMC Bayesian inference phylogeny of Amietophrynus gutturalis derived from the ND2 mtDNA marker.

Maximum Likelihood bootstrap values greater than 70% are shown above and Bayesian posterior probabilities greater than 0.7 are shown below branches at terminal nodes.

Figure 3.3: TCS haplotype network from the 16S rRNA marker for Amietophrynus gutturalis.

Dashes on the network indicate single nucleotide polymorphisms and the nodes represented by black circles indicate inferred missing haplotypes. The circles are proportional to the amount of samples represented for each haplotype.

All invasive samples from the Cape Town and Mauritius populations and the natural population are represented on the inset maps with the legend indicating which clade they represent. The colours represented in the legend correspond with those represented by the haplotype network. Numbers in the haplotypes are represented in Table 3.1.

Figure 3.4: TCS haplotype network from the ND2 mtDNA marker for Amietophrynus gutturalis.

All samples from the natural range and both the Cape Town and Mauritius invasive populations are included and indicated on the inset maps.

Dashes in the network represent single nucleotide polymorphisms between haplotypes and black circles represent inferred missing haplotypes. The circles in the networks are proportional to the number of samples representing each

–  –  –

The Bufonidae are well researched and there is  a thorough understanding of most species life   histories. Bufonidae systematics have been   recently revised (Frost, 2015) and there has been a renewed interest in biogeographical studies (Froufe et al., 2009; Vasconcellos et al., 2010;

Portik & Papenfuss, 2015). Although there was a focus on bufonid evolution during the 1960’s and 1970’s (Tihen, 1962; Blaire, 1972; Tandy, 1972), there remain major gaps in the understanding of their historical biogeography. With the advent of modern molecular techniques it is now possible to investigate this at a deeper level.

The Amietophrynus genus comprises 44 Figure 1.1: Photograph of the guttural currently recognized species (Frost, 2015). They toad, Amietophrynus are widely distributed across Africa and parts of gutturalis, Power 1927.

the Middle East (Frost, 2015). Many species within the genus are common, have a broad geographic distribution and exhibit a generalist life history strategy. Even though much is known about the guttural toad, Amietophrynus gutturalis (Fig. 1.1), there has been renewed interest in the species due to the successful establishment of invasive populations outside of their natural range. Furthermore, no research has been conducted on the population genetics of the species. In order to manage invasive species adequately, it is important to have a clear understanding of their life history, their abilities to hybridize and their evolutionary history. Although a multi-species molecular study (Cunningham & Cherry, 2004), which included A. gutturalis, has already been conducted, a species specific investigation of the natural and invasive populations is yet to be completed.

Background on Amietophrynus gutturalis The guttural toad, Amietophrynus gutturalis (Fig. 1.1), is a large (up to 140 mm SVL) common and widespread species which garners its name from its loud guttural advertisement call (Channing, 2001). The species wide distribution includes Angola, Botswana, The 12 Democratic Republic of Congo, Kenya, Lesotho, Malawi, Mozambique, Namibia, Somalia, South   Africa, Swaziland, Tanzania, Zambia and   Zimbabwe (Channing 2001; du Preez et al., 2004; IUCN, 2013), but is absent from the arid   regions of western Botswana, southern Namibia   and southern South Africa (Fig. 1.2) (Channing, 2001). This generalist toad is found in a wide variety of habitats from sea level to ~1 900 m (Channing, 2001; du Preez et al., 2004). It is a highly adaptable species and can be found in an assortment of savannahs, grasslands, thickets, agricultural lands and it readily adjusts to Figure 1.2: Distribution map of A. gutturalis urban areas where it often inhabits garden across Africa (adapted from the IUCN Red List).

ponds (Channing, 2001; du Preez et al., 2004).

They are active nocturnally and take refuge during the day under logs, rocks, in gutters and drain-pipes, and burrows or holes that they excavate in soft ground (du Preez et al., 2004).

Guttural toads are prolific breeders and a single pair is able to deposit between 15 000 and 25 000 eggs in a single clutch (Wager, 1986; Channing, 2001; du Preez et al., 2004). Two gelatinous strings of eggs are laid in shallow water at the edge of pools, and are often wound in and around vegetation (Channing, 2001). In the tropical and sub-tropical regions of the species range, they are able to breed year round and females will often produce two clutches.

However, in the more temperate southern regions of their range, they reproduce seasonally (Channing, 2001; du Preez et al., 2004), during the warm, wet summer months.



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