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Chapter1 Foraging Ecol KL Mmonwa Evolution and foraging ecology of patellid limpets Molecular phylogeny, phylogeography and evolutionary adaptation of foraging behaviour amongst sympatric patellid limpets along the southern African shoreline A thesis submitted in fulfillment of the requirements of the degree of Doctor of Philosophy (Marine Biology) of Rhodes University South Africa by Kolobe Lucas Mmonwa September 2013 Supervisor: Prof. C.D. McQuaid (Distinguished Professor, Chair of Zoology and SARCHI Research Chair in Marine Ecosystem Research, Rhodes University) Co-Supervisor: Prof. N.P. Barker (Head of Botany Department & Molecular Ecology and Systematics Group, Rhodes University) KL Mmonwa Evolution and foraging ecology of patellid limpets “In whom are hidden all the treasures of wisdom and knowledge” (Colossians 2:3, ZCC Family Bible) “I am fully in the know that the earth moves at about 100, 000 km/h around the sun, 1000 times faster than the speeds we go at on a highway, but I am not confused who God is” The Honourable His Grace The Right Reverend Bishop Dr. BE Lekganyane (Taung: Northwest Province, 11th March 2012) “All religions, arts and sciences are branches of the same tree” Albert Einstein (1879 – 1955) “Gravity explains the motions of the planets, but it cannot explain who set the planets in motion” Sir Isaac Newton (1642 – 1727) KL Mmonwa Evolution and foraging ecology of patellid limpets ABSTRACT The southern African shoreline is inhabited by a great diversity of patellid limpets of which most are endemic to South Africa. These limpets have evolved foraging mechanisms that partition ecological resources and reduce interspecific competition, resulting in ecological specialists and generalists. The evolution of ecological specialization or generalization remains poorly understood and there is no agreement on how such evolutionary transitions are correlated with levels of genetic diversity. This study investigated evolutionary correlations between territoriality in foraging and genetic structure of southern African patellid limpets (Cymbula and Scutellastra spp.) using stable δ13C and δ15N ratios, mitochondrial and nuclear DNA markers. The outcomes of the study were best rationalized and understood in the context of the scale of analysis in terms of both space and taxonomy. At biogeographic scales and the interspecific level, the stable isotope signatures and genetic structure of these limpets are determined by extrinsic factors such as biogeography and oceanography. However, at the smallest site scales and the intraspecific level, the isotope signatures and genetic diversity of these limpets are significantly correlated to their foraging traits. At large scales, there are no correlations between foraging behaviour and either genetic structure or isotope signature. At smaller scales, territorial Scutellastra foragers display both isotopic enrichment and greater haplotype diversity than congeneric non-territorial foragers. Thus, the isotope signatures and genetic structure of these limpets are determined by intrinsic species-specific response linked to their foraging behaviour. However, this pattern was intriguing as differences between territorial and non-territorial limpets in both isotopic signature and genetic diversity were observed only along the south coast when the same species were compared in other biogeographic regions. The significant interaction effect between foraging behaviour and stable isotope signatures was only observed from the sites within the Agulhas Bank or which are strongly influenced by the Agulhas current. This south enrichment in isotopic ratios is due to the mixing differences between onshore and offshore waters as the Agulhas current moves from east to south. iii KL Mmonwa Evolution and foraging ecology of patellid limpets At the generic level, the correlation between foraging behaviour and isotope signatures and genetic structure were particularly profound for Scutellastra species. The molecular phylogeny revealed deep evolutionary divergence between territorial and non-territorial Scutellastra spp. This divergence was concordant with morphological differences in shell shape and radula anatomy between territorial and non-territorial species. A taxonomic review of the scutellastrid spp. is proposed, suggesting possible re-consideration of the genus as two genera characterized by either territoriality or non-territoriality. The divergence between territorial and non-territorial species in both Scutellastra and Cymbula took place approximately in the early Oligocene. Major climatic cooling and decreases in sea level occurred during the Oligocene and this probably exposed much of the lower intertidal zone, increasing new potential habitats and algal availability. The Oligocene exposure of rocky shores and algal abundance in the lower intertidal zone probably elicited resource partitioning amongst these patellid limpets and subsequently, the evolution of territorial and non-territorial species. Analyses of the demographic history of these patellid limpets revealed evidence of post-glacial spatial expansion around the Pleistocene, implying these limpets were at population equilibrium during the dramatic LGM sea temperatures. Thus, these limpets managed to expand their range during dynamic oceanographic oscillations and dramatic sea-level changes in the Pleistocene. This study highlighted the importance of applying ecological traits as a subject to investigate and comprehend the evolutionary ecology of marine herbivores. The foraging traits of these true limpets are reflected in both their stable isotope ratios and genealogy, presumably as an evolutionary consequence of competition. iv KL Mmonwa Evolution and foraging ecology of patellid limpets ACKNOWLEDGEMENTS Rhodes University was my home away from home for the past six years. I had friends and folks who acted as my family making this stay-away from home enjoyable and memorable. Thus, there are lots of people who directly or indirectly contributed to the success of this thesis and I am not apologetic for the long length of this acknowledgements. Foremost, let me convey my sincere gratitude to my supervisors, Prof. Christopher McQuaid and Prof. Nigel Barker. You both believed in me and provided me with the opportunity to unravel some of the complex yet interesting research questions in evolutionary biology. Prof McQuaid, I always knew my grammar would receive severe scrutiny every time I had to hand in thesis drafts. I am grateful for your constructive criticism which kept me on my toes to keep learning - thank you! Collecting algal and limpets samples was always a challenge considering a long stretch of the South African coastline and distances amongst the study sites. The following people willingly and unconditionally collected and provided limpets samples from various sites along the southern African coastline. Prof. George Branch, I am grateful for the limpet’s samples you collected from the almost unreachable west coast sites and also for providing samples of Scutellastra miliaris from the Angolan shoreline. Most importantly, you are greatly thanked for those brain storming discussions, giving suggestions on adding more study species and possible research questions I could attempt to answer. Dr. Peter Teske, you did not only motivate me to become a workaholic lab rat, but your 12 hours` presence in the lab inspired me to produce a total of 1000 DNA sequences! I would sincerely like to thank you for your inputs on molecular genetics, especially suggesting the application of nuclear intron makers, yes they worked! Lastly, I know I was for the good course capitalizing on your field trips, and thank you for those limpet samples from the northern Kwazulu-Natal coast. v KL Mmonwa Evolution and foraging ecology of patellid limpets Dr. Chris Kelly, what else can I says my brother, thank you! The enthusiasm, tireless and unconditional efforts and humanity you showed towards my work will never be forgotten. These ranged from digs relocation, lab equipments, primer design, phylogenetic analyses and of course exchanging words on the Kingdom of God!!! Indeed God wrote only two fundamental books, the Bible and the Creation! Dr. Syd Rahmdani and Dr. Sandun Perera, together you made it possible for me to sample the east coast. The time spared, sacrificing your own working hours, the transport you provided, logistics made to secure me lab space at the University of KwaZulu-Natal (Westville Campus), field photos taken…all are warmly appreciated! The commitment you showed towards my work was superb; sometimes it looked like this was your own work. I am really indebted to you guys! Dr. Sven Kaehler of the IsoEnvironmental Lab, Rhodes University, you solely made the stable isotope analyses possible, thank you! In spite of keeping on sending you with more and more samples to analyse, you were always there when needed and met the deadlines when it was seemingly impossible. Finally, a very big thank you for leaving that lab unlocked overnights; ultimately I got rewarded for those sleepless nights I spent there! Dr. Franchesca Porri, you are sincerely thanked for your immediate assistance with the stable isotope analyses, the inputs and suggestions you proposed were really helpful, thank you! Dr. Victoria Cole, the literature you provided on the review of phylogeny of patellogastropods was very helpful, chapter one was almost moulded around that article, thanks! Dr. Nicodemus Mahutsa and Stacey Weeks, I am grateful for the understanding, patience and commitment you had shown
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