The potential of bats as bioindicators for areas currently transformed by opencast mining within the Vhembe Biosphere Reserve, Limpopo Province, South Africa.

PhD (Zoology)

Department of Zoology

Bats are the second most diverse order of mammals and provide crucial ecosystem services from insect control (including significant crop pest species), to pollination of plants and seed dispersal. Bats are known to be sensitive to alterations in their environment. Globally, bat populations and communities are under pressure due to anthropogenic activities that alter their natural habitats creating unfavourable habitats for some bat species and favourable conditions for others. Anthropogenic activities, impose a multitude of impacts on bats such as artificial lighting throughout nocturnal periods and excessive noise during both diurnal and nocturnal periods. These alterations of habitats affect bat roosting and emergence behaviour, disrupt commuting routes to foraging grounds and alter interspecific competition. Additionally, bats are exposed to and suffer physiological issues relating to contaminants such as heavy metals and trace elements of which their liberation is exacerbated by human activities. African bat conservation is already under considerable pressure from the development occurring throughout the continent. A looming development of significant concern is the proposed African Mining Vision to develop mining and transport networks throughout sub-Saharan Africa. The fate of bat conservation in Africa is dependent on bat taxonomy (with new species regularly described), an understanding of African bat ecology and the responses of bat species to changes in their environment. Research covering these aspects are greatly needed in order to propose environmental mitigation and remediation strategies. Bats have the potential as bioindicators to provide information concerning ecosystem health pre-, during and post- large scale developments such as mining. My study focused on how a bat community in northern Limpopo Province was impacted by the de Beers Venetia opencast diamond mining operation. I investigated which bat species have the potential to be bioindicators based on the impact of habitat degradation (Chapter 2). The impact of artificial light and anthropogenic noise was explored (Chapter 3) and the use of bat fur and blood as biomarkers of bat exposure to heavy metals and trace elements (Chapter 4). Bats have the potential to be good bioindicators as they are easy to monitor in areas like mines that are often a challenge to access and or have high safety risks due to heavy machinery movement and human exposure to possible environmental contaminants. By using passive acoustic recording techniques, the composition and activity of the bat community was determined on the Venetia diamond mine and over the natural areas neighbouring the mine. Six bat detectors were deployed for a full summer and winter season to determine what factors (both anthropogenic and natural) influenced total bat activity as well as species richness and diversity. The effect of habitat type (natural habitats Musina Mopane Bushveld and Limpopo Ridge Bushveld vs altered landscapes of the wastewater dam and opencast pit), season, minimum temperature (Tmin) and moon phase were investigated. Habitat type and season were shown by the best-fit models to be the main factors affecting bat activity, which was lower during winter and consistently lower over the heavily disturbed opencast mining pit. It was evident from the passive acoustic recordings of echolocation calls that the Venetia diamond mine was an important resource for numerous bat species, particularly at the wastewater dam, boasting ~18 out of 22 species/species groups. The wastewater dam provided a sought after resource for foraging and possibly drinking by bats. The infrastructure of the mine was also observed to be used by molossid bats as roosting opportunities. Based on the clear-cut response of three species/species groups to habitat type, Laephotis capensis/Pipistrellus (Vansonia) rueppellii, Afronycteris nana and Pipistrellus rusticus/Neoromicia anchietae were proposed as bioindicators on the Venetia diamond mine. All three species/species groups could be environmental indicators which means that they respond to physical changes in the environment, in this case, changes in preferred habitat. Laephotis. capensis/P. rueppellii generally avoided the mining footprint and were abundant in the natural areas whereas A. nana and P. rusticus/N. anchietae were prolific over the wastewater dam, particularly during winter. The response of A. nana and P. rusticus/N. anchietae may be a reflection of changes in insect species composition over the wastewater dam in relation to potential changes in water quality and as such, have also been suggested as ecological indicators as they may be reflecting the change in another taxon or group (invertebrates). Further research in this regard is required. Bat species were characterised as exploiters and adapters to resources provided by the mine such as new artificial roosting opportunities in infrastructure and resource creation, particularly artificial water sources that would otherwise be scarce for bats in the semi-arid environment. Examples of these exploiter and adapter species were Chaerephon pumilus/Mops condylurus that exploited resources provided by the mine from roosting in buildings to using the wastewater dam, and P. hesperidus as an adapter that used the wastewater dam as an important resource particularly during winter and was only recorded in natural areas during summer but is not known to roost in the infrastructure of the mine. Even though the mining activities provided resources, bats were exposed to continuous anthropogenic noise and artificial light during their night-time foraging period. To investigate the impacts of anthropogenic noise and artificial lighting, a transect was installed on the Venetia diamond mine using six SM4BAT acoustic recorders (bat detectors) (Wildlife acoustics, Inc.) to passively record bat species and their associated activity. The transect began in a brightly lit area near some workshops and a conveyor belt system and extended past the well-lit and noisy processing plant, into an open-air laydown storage area and terminated in natural vegetation. Surprisingly, according to mixed-effects models, in general, anthropogenic noise did not have a significant impact on bat activity or species richness. Artificial light only negatively impacted foraging activity and there was little evidence of bats foraging under the floodlights near the workshop and processing plant. Artificial light may possibly impact total bat activity and searching/commuting behaviour. In support of the data concerning the lowest bat activity and species richness over the habitat devoid pit of the mine, the percentage of natural vegetation cover was the most important factor influencing all bat activity and species richness. With significant bat activity recorded over the mine wastewater dam, there is potential for bats to be exposed to high concentrations of contaminants, particularly heavy metals and trace elements that would otherwise be naturally occurring at lower concentrations in the environment. Therefore, I investigated the potential bioaccumulation of elements in molossid bats from the mining footprint and in a control area adjacent to the mine. There is great interest in using bats as bioindicators of environmental contaminants and with a focus on non-lethal and less invasive methodologies, the fur and blood of several Tadarida aegyptiaca and C. pumilus/M. condylurus was tested for 23 elements. Fur is a good indicator of exposure to elements over an extended period and blood provides insight into more recent exposure. Fifteen of the 22 elements (barium excluded as it was predominantly below detection limits), were higher in the fur that in the blood samples. Concentrations of boron (B), potassium (K), rubidium (Rb) and cadmium (Cd) in fur and zinc (Zn), and mercury (Hg) in blood were significantly higher in samples from the opencast diamond mine compared with the control site. Manganese (Mn) was higher in the blood of bats from the control site than from the mine. Although weak, the only significant correlations between fur and blood element concentrations were found for Hg and strontium (Sb). Comparative data with other bat species is scant in the literature and there are currently no toxicological thresholds for elements in bats, thus the low concentrations of most elements, except aluminium (Al), iron (Fe) and Zn, may reflect background values. These data are the first presented to compare blood and fur elemental concentrations of South African bats the implications of which are currently unknown. 3 These data presented in my thesis has great potential to add to the environmental monitoring of the Venetia diamond mine by providing insight into trends in the bat population (including species richness) that utilise the mine associated (drinking and foraging areas over the waste water dams, and roosting opportunities in mine infrastructure). These data can be used as a baseline to monitor the current and future environmental impacts of the mine as production continues and, can be used to monitor and assist rehabilitation efforts soon to be underway.

NRF