Evaluating the effects of biogeography and fragmentation on the taxonomic, functional, and genetic diversity of forest-utilising bats in a South African biodiversity hotspot

Moir, Monika Ilka (2020-12)

Thesis (PhD)--Stellenbosch University, 2020.

Thesis

ENGLISH ABSTRACT: Bats are a highly diverse mammalian order and are some of the most economically important non-domesticated vertebrates, providing many ecosystem services that contribute to the global economy. Yet, they remain a largely understudied taxon, particularly in the Eastern Cape province of South Africa, in which basic surveys of bat assemblages utilising indigenous forests are lacking. Indigenous forests constitute South Africa’s smallest and most fragmented biome yet support disproportionally high biodiversity. They have been fragmented throughout most of their evolutionary history due to global palaeoclimatic shifts; the responses of bats to forest fragmentation and historical climatic shifts in this habitat have been poorly studied. This study addresses these gaps with the broad aims of compiling a species inventory from 17 forests across the Eastern Cape and KwaZulu-Natal provinces; assessing the effects of fragmentation and biogeography on taxonomic and functional diversity of bat assemblages; and determining how genetic diversity and population genetic structure are informed by forest habitat associations and fragmentation. A multi-faceted approach of sampling methods, including capture and acoustic recording, and species identification techniques (morphology, acoustics, and DNA barcoding) were used to assemble an inventory of 25 species, with range extensions noted for six species. The first reference call library of hand released bats for forests in this region is presented, which may be used for species identification in further acoustic surveys. A minimum acoustic monitoring period of 6 to 7 nights per forest is recommended for future surveys. Forest biogeography was an important determinant of the functional diversity of insectivorous bat assemblages. Forest edge effects were found to demonstrate a positive relationship with functional evenness, thus motivating for maintenance and conservation of forest edges, particularly in temperate regions. Larger forearm length and low wing loading were identified as morphological traits exhibiting greater sensitivity to fragmentation, flagging species exhibiting these traits as potentially vulnerable to habitat fragmentation. The effect of historical climate-induced fluctuations of forest extent on population genetic structuring and demographic histories for six species was investigated using two mitochondrial markers, cytochrome b and D-loop. Population genetic trends were not informed by forest habitat associations, but rather by species-specific traits of dispersal ability, philopatry, and roost utilisation. Low genetic diversity and high population structure identify two species, Rhinolophus swinnyi and Laephotis botswanae, for conservation priority. Demographic responses to the Last Glacial Maximum (LGM) were not detected, with all six species displaying population expansions over this time. It appears that volant insectivores in eastern South Africa were less affected by the harsh conditions of the LGM than elsewhere. The dusky pipistrelle (Pipistrellus hesperidus) was used as a model organism to investigate the gene flow, genetic diversity, and migration of a forest-utilising species across the region with the use of eight microsatellite markers. The effects of urbanisation and agricultural development on gene flow were also examined. Findings of low population structure, low migration rates, and two genetic discontinuities were presented. This species does not depict dependence on forested habitats to maintain genetic connectivity on the landscape. The data also suggest that agricultural development and urbanisation have not yet had an impact on gene flow, thus providing a baseline with which to monitor the effects of future anthropic development on this species. Overall, this study has provided novel insights into the taxonomic, functional, and genetic diversity of forest-utilising bats in relation to biogeographical history and fragmentation within eastern South Africa

AFRIKAANSE OPSOMMING: Vlermuise is 'n baie diverse soogdierorde en is van die mees ekonomies belangrike nie-domestiese gewerwelde diere, wat baie ekosisteemdienste lewer en sodoende bydra tot die wêreldekonomie. Tog bly hulle 'n grootliks onderbestudeerde takson, veral in die Oos-Kaap en KwaZulu-Natal provinsies van Suid-Afrika, waar basiese opnames oor vlermuis samestellings ontbreek. Inheemse woude vorm die kleinste en mees gefragmenteerde bioom van Suid-Afrika, maar nogtans ondersteun dit ‘n buitensporige hoë biodiversiteit. Hulle is deur die grootste deel van hul evolusionêre geskiedenis gefragmenteer as gevolg van wêreldwye paleoklimatiese verskuiwings; die reaksie van vlermuise op woudfragmentering en historiese klimaatverskuiwings in hierdie habitat is swak bestudeer. Hierdie studie spreek hierdie leemtes aan met die breë doelstellings om 'n spesies-inventaris vanaf 17 woude regoor die Oos-Kaap en KwaZulu-Natal provinsies saam te stel; die gevolge van fragmentasie en biogeografie op taksonomiese en funksionele diversiteit van vlermuis samestellings te evalueer; en vas te stel hoe genetiese diversiteit en genetiese struktuur van die populasie bepaal kan word deur woud habitat assosiasies en fragmentasie. 'n Veelsydige benadering van monsternemingsmetodes, insluitend vang- en akoestiese opname, asook spesie-identifikasietegnieke (morfologie, akoestiek en DNS-strepieskodering) is gebruik om 'n inventaris van 25 spesies saam te stel met uitbreidings in geografiese omvang aangeteken vir ses spesies. Die eerste biblioteek met roep verwysings vir hand vrygestelde vlermuise van woude in hierdie streek word aangebied wat in verdere akoestiese opnames gebruik kan word vir die identifisering van spesies. 'n Minimum akoestiese moniteringstydperk van 6 tot 7 nagte per woud word aanbeveel vir toekomstige opnames. Die biogeografie van ‘n woud was 'n belangrike bepalende faktor van die funksionele diversiteit van insekvretende vlermuise. Daar is gevind dat woud rand-effekte 'n positiewe verwantskap met funksionele egaligheid toon en bied dus motivering vir die instandhouding en bewaring van woud rande veral in gematigde streke. Groter voorarmlengte en lae vlerklading is geïdentifiseer as morfologiese eienskappe wat meer sensitiwiteit getoon het vir fragmentasie wat sodoende spesies wat hierdie eienskappe toon as potensieel kwesbaar vir fragmentasie van die habitat uitlig. Met behulp van twee mitokondriale merkers, sitokroom b en D-lus, is die effek van historiese klimaat-geïnduseerde wissellinge van die omvang van die woud op die genetiese strukturering en demografiese geskiedenis van die populasie vir ses spesies ondersoek. Populasie genetiese neigings is nie deur woud habitat assosiasies gevorm nie, maar eerder deur spesiespesifieke eienskappe van verspreidingsvermoë, filopatrie en nes gebruik. Lae genetiese diversiteit en hoë populasie struktuur identifiseer twee spesies, Rhinolophus swinnyi en Laephotis botswanae, vir prioriteitsbewaring. Demografiese reaksies op die Laaste Glasiale Maximum (LGM) is nie opgespoor nie met al ses spesies wat gedurende hierdie tyd uitbreiding in populasie getoon het. Dit lyk asof vlieënde insekvreters in oos Suid-Afrika minder geraak is deur die haglike toestande van die LGM as elders. Die Kuhl-vlermuis (Pipistrellus hesperidus) is as 'n modelorganisme gebruik om die geenvloei, genetiese diversiteit en migrasie van 'n woud-bruikende spesie oor die hele streek te ondersoek met behulp van agt mikrosatellietmerkers. Die gevolge van verstedeliking en landbou ontwikkeling op geenvloei is ook ondersoek. Bevindinge van lae populasie struktuur, lae migrasietempo, en twee genetiese diskontinuïteite word aangebied. Hierdie spesie toon nie ‘n afhanklikheid van bewoude habitatte om genetiese konnektiwiteit in die landskap te handhaaf nie. Die data dui ook daarop dat landbou ontwikkeling en verstedeliking nog nie 'n invloed op geenvloei gehad het nie wat dus 'n basis bied om die gevolge van toekomstige antropiese ontwikkeling te montior op hierdie spesie. Hierdie studie lewer as geheel nuwe insigte tot die taksonomiese, funksionele en genetiese diversiteit van woud-bruikende vlermuise in verband met biogeografiese geskiedenis en fragmentasie in oos Suid-Afrika.

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