Biodiversity in Southern Africa

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Biodiversity is important for sustaining life on Earth yet it is threatened globally. The BIOTA Southern Africa project analysed the causes, trends, and processes of change in biodiversity in Namibia and western South Africa over nearly a full decade, from 2001 until 2010. This book, which is comprised of three volumes, offers a summary of the results 9 7 8 from 3 9 3 3the 1 91 many 77 84 35 98 3and 3 1 diverse 17458

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subprojects during this ﬁrst period of long-term observation and related research, at both local and regional scales, and with a focus on sustainable land management options for the region.

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2 Patterns and Processes at Regional Scale KLAUS HESS PUBLISHERS

ISBN-Namibia

Biodiversity in Southern Africa

Namibia ISBN Namibia ISBN

Biodiversity in Southern Africa Vol. 2

Patterns and Processes at Regional Scale

© University of Hamburg 2010 All rights reserved Klaus Hess Publishers www.k-hess-verlag.de

ISBN all volumes: 978-3-933117-44-1 (Germany), 978-99916-57-30-1 (Namibia) ISBN this volume: 978-3-933117-46-5 (Germany), 978-99916-57-32-5 (Namibia) Printed in Germany

Suggestion for citations: Volume: Schmiedel, U., Jürgens, N. (2010) (eds.): Biodiversity in southern Africa 2: Patterns and processes at regional scale. Göttingen & Windhoek: Klaus Hess Publishers. Article (example): Petersen, A., Gröngröft, A., Mills, A., Miehlich, G. (2010): Soils along the BIOTA transect. – In: Schmiedel, U., Jürgens, N. (eds.): Biodiversity in southern Africa 2: Patterns and processes at regional scale: 84–92. Göttingen & Windhoek: Klaus Hess Publishers. Corrections brought to our attention will be published at the following location: http://www.biota-africa.org/biotabook/

Cover photograph: Giraffes on the game farm Omatako Ranch (Observatory S04 Toggekry) in the Namibian Thornbush Savanna. Photo: Jürgen Deckert, Berlin/Germany. Cover Design: Ria Henning

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Article III.6.1 – Author’s copy – Please cite this article as follows: Musil, C., Nyaga, J., Maphangwa, K., Raitt, L. (2010): Responses of dwarf succulent plants, lichens, and soils to experimental climate warming in an arid South African ecosystem. – In: Schmiedel, U., Jürgens, N. [Eds.]: Biodiversity in southern Africa. Volume 2: Patterns and processes at regional scale: pp. 246–250, Klaus Hess Publishers, Göttingen & Windhoek.

Experiments

Responses of dwarf succulent plants, lichens, and soils to experimental climate warming in an arid South African ecosystem CHARLES MUSIL*, JUSTINE NYAGA, KHUMBUDZO MAPHANGWA & LINCOLN RAITT

Summary: The effects of daytime passive heating averaging 3.8°C above ambient, achieved with clear acrylic hexagonal open-top chambers, on the vegetation and soils in an acknowledged centre of floral diversity and endemism in the arid southern bioregion of the South African Succulent Karoo Biome was examined. After 12–months warming, populations of all eight dwarf succulent species examined displayed diminished numbers of live leaves (increased leaf mortalities), the effects more prominent in small, sparsely branched species with single leaf pairs than larger, shrubby or creeping species with multiple leaves. Similarly, the four lichen species examined displayed diminished photosynthetic quantum yields in response to experimental warming, which were of much greater magnitude than the reductions in numbers of live leaves measured in the dwarf succulents indicating that lichens may provide more sensitive indicators of climate change. Substantially higher soil CO2 effluxes were measured in soils with moderate than sparse vegetation cover, but the experimental warming had only small statistically insignificant effects on soil CO2 effluxes. It is concluded that even mild anthropogenic warming is likely to exceed the thermal thresholds of many southern African lichens and quartz field succulent plants leading to metabolic impairment and increased likelihood of localised extinction. Also, arid ecosystem soils are likely to have a minor impact on atmospheric CO2 with global warming as they are relatively small sources of CO2 emissions.

Introduction The unprecedented accumulation of carbon dioxide and other greenhouse gases in the atmosphere since pre-industrial times has already had a discernible influence on global temperature and is forecast to cause further warming this century (IPCC 2007). Diminished plant productivities in response to increased temperatures in experimental warming trials have been reported in Forest, Grassland, high and low latitude/altitude Tundra biomes (Rustad et al. 2001) implying that plant productivity could be expected to decrease further in subtropical and tropical ecosystems. However, there are few data on plant and lichen 246

responses to climate warming in arid subtropical ecosystems, especially in the southern African Succulent Karoo Biome listed among 34 global biodiversity hot spots (Myers et al. 2000). Here, current thermal regimes for many of the almost 1,600 endemic succulent species of the subfamily Ruschioideae, which rapidly diversified in the region during the cooler Pleistocene period (Klak et al. 2004), are likely closely proximate to their tolerable extremes. Apart from the flora, soils are the major reservoir of carbon in terrestrial ecosystems, containing more than two-thirds of the total carbon in the terrestrial part of the biosphere (Lin et al. 1999). The flux of carbon from soils to the atmosphere B IODIVERSITY

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in form of carbon dioxide accounts for about 25% of the global CO2 exchange (Jia & Zhou 2008). Almost 10% of the atmosphere’s CO2 passing through soils each year, which is more than 10 times the CO2 released from fossil fuel combustion (Schlesinger & Andrews 2000, Raich & Tufekcioglu 2000). A variety of temperature-manipulation experiments around the world have shown that soil respiration generally increases with warmer temperatures in relatively wet soils (Zhou et al. 2006) with small climatic-induced changes in soil respiration (20% for a 6.0°C increase) expected to have large effects on atmospheric CO2 concentrations with potential feedbacks to climate change (Reichstein et al. 2003, Sánchez et al. 2003). The focus on soil carbon fluxes has mainly been in tropical ecosystems due to their dominant contribution to global carbon emission budget (Adachia et al. 2006) but there are few data on gaseous carbon emissions in arid ecosystems, which though low at a global scale do exhibit huge pulses during intermittent wet phases (Amy et al. 2004). In view of these deficiencies in knowledge, the potential impacts of climate warming approximating a future climate scenario on the flora and soil carbon exchange were tested experimentally in an arid South African ecosystem. The study forms a component of a BIOTA Phase III overarching theme, which seeks to assess the current state and monitor the intensity and direction of change of biodiversity.

Methodology The study area was the arid southern bioregion of the South African Succulent Karoo Biome, known locally as the Knersvlakte, which is an acknowledged centre of floral diversity and endemism

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(Hilton-Taylor 1996). Daytime passive heating of the natural vegetation and soils was achieved with clear acrylic hexagonal open-top chambers 120 cm in diameter and 50 cm high (Fig. 1A). Demarcated plots of equivalent open-top chamber dimensions enclosed by 40 cm high steel fencing with a 5 cm diameter mesh comprised the controls, which represented ambient conditions. At the centers of the open top warming chambers and control plots, polyvinyl chloride (PVC) soil collars with an internal diameter of 10 cm and a length of 5 cm were buried to a depth of 4 cm for soil carbon flux measurements. Also installed in the open top chambers and control plots were atmospheric, soil temperature and moisture sensors interfaced with miniature loggers, set to record hourly, mounted in radiation shields (Watch Dog 450, Spectrum Technologies Inc., Plainfield, Illinois, USA). The average 3.8°C temperature increase above ambient measured in the open top warming chambers closely approximated the mean annual temperature increase of 4.5°C (means of 7 GCM models) predicted by the SRES A2-high climate sensitivity scenario for the Succulent Karoo Biome towards the end of the century (Hulme et al. 2001). Sixty experimental warming chambers and control plots were randomised on substrates overlaid with quartz-gravel and shale, phyllite and limestone with different vegetation cover and composition at the beginning of winter to allow gradual acclimation of the flora and soil microorganisms to the artificially elevated temperatures. The floral species included in six or more of the experimental warming chambers and control plots included the lichens Xanthoparmelia austroafricana, Xanthoparmelia hyporhytida, Xanthoparmelia spp. (un-described) and Xanthomaculina hottentotta, and the common dwarf succulent plants Oophytum oviforme, Conophytum minutum var. minutum, Agyroderma pearsonii, Cephalophyllum spissum, Dactylopsis digitata, Cephalophyllum framesii, Drosanthemum diversifolium and Ruschia burtoniae. Responses of the dwarf succulent plant species to the experimentally elevated temperatures were determined at 3-monthly intervals. Photographs of the

Fig. 1: Measuring climate warming impacts on the vegetation and soils in the arid South African Succulent Karoo Biome. A: Clear acrylic hexagonal open-top warming chamber with miniature data loggers connected to soil moisture and temperature sensors. B: Photographing succulent plant populations with high resolution digital camera. C: Khumbudzo Maphangwa measuring photosynthetic quantum yields of lichens with modulated fluorescence meter. D: Justine Nyaga measuring soil respiration with an infrared gas analyzer.

succulent plant populations present in each chamber and control plot were obtained with a high resolution, three-band Foveon X3 sensor, Sigma SD10 digital camera suspended above the chambers and control plots (Fig. 1B). The numbers of visibly live leaves present on each dwarf succulent plant species in each chamber and control plot were precisely determined with the aid of image analysis software (Image-J ver.1.34I, National Institute of Health, USA: http://rsb.info. nih.gov/ij/). These were summed for the entire species population in each chamber and control plot and expressed on a uniform m² basis. Responses of the lichen species to the experimentally elevated temperatures were determined between 08h00 and 10h00 at monthly intervals. The lichens in each chamber were hydrated with 50 ml of water applied as a fine mist spray and their photosynthetic quantum yields at a steady-state determined with a modulated fluorescence meter (OSI-F1, OptiSciences Inc., Hudson, USA) following a 0.8 s light pulse of 15,000 μE (Fig. 1C). Responses of soil carbon flux to the experimentally elevated temperatures were determined at monthly intervals. Four measurements of soil CO2 efflux

KNOWLEDGE THROUGH EXPERIMENTS

spaced two hours apart were taken inside the polyvinyl chloride (PVC) soil collars within each top warming chamber and control plot (Fig. 1D) with a portable Li-Cor 8100 infrared gas analyzer (Li-Cor BioSciences, Lincoln, Nebraska, USA). Measured soil respiration rates as μmol CO2 m-2 s-1 were averaged for the day and converted to g CO2 m-2 d-1.

Statistical analyses All measurements were loge transformed before statistical analysis to reduce the inequality of variance in the raw data. As the experimental designs were not fully balanced, a REML (residual maximum likelihood) variance component analysis (repeated measures mixed model) was applied to test for significant effects of warming using the Wald Х² statistic generated by REML. Warming treatment and either succulent plant species, lichen species or soil vegetation type were fitted in the fixed model and season and measured plant, lichen or soil variables in the random model. Differences exceeding twice the mean standard errors of differences were used to separate 247

Experiments Fig. 2: Seasonal responses to experimental warming of eight dwarf succulent plant species, four lichen species and soils from three different soil vegetation units, viz: quartz-gravel substrates with sparse vegetation cover (QSV), and shale, phyllite and limestone derived substrates with sparse vegetation cover (SSV) and moderate vegetation cover (SMV). Predicted means with non overlapping standard error bars significantly different at p ≤ 0.05.

significantly different treatment means at p ≤ 0.05. This based on the fact that for a normal distribution from REML estimates, the 5% two-sided critical value is two.

Results and discussion Populations of all eight dwarf succulent species displayed significantly (p ≤ 0.05) diminished numbers of live leaves (increased leaf mortalities) in response to experimental warming, which were of greatest magnitude in late autumn 12-months after open top warming chamber placement (Fig. 2). Small, sparsely branched succulent plant species comprising single, highly connate, spheroid leaf pairs per axis, such as O. oviforme, C. minutum, and A. pearsonii, exhibited much greater decreases in numbers of live leaves (range: 33.8% to 68.4%) than 248

populations of larger, shrubby or creeping species with multiple leaves, such as C. framesii and R. burtoniae (range: 9.1% to 13.7%). These differences explained by the much higher air temperatures leaves of small unbranched species located at or close to the soil surface were exposed to than larger branched shrubby species with multiple leaves elevated above the soil surface. In fact recorded soil surface temperature extremes in the open-top chambers of 54.8°C were close to the temperature threshold of 55°C considered tolerable by most vascular plants (Kappen 1981). Higher thermal thresholds (range: 66.4°C to 70.0°C) have been reported in a diverse array of succulents (Nobel 1989). However, thermal thresholds of southern African specialised dwarf succulent forms are allegedly lower due to the milder thermal regimes (up to 3°C lower) they experience on the highly reflective quartz B IODIVERSITY

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substrates (Schmiedel & Jürgens 2004). This suggestion supported by the abrupt decline in the activation state of the photosynthetic enzyme Rubisco measured in one dwarf succulent C. spissum from around 90% to 92% at temperatures between 40°C and 52°C to about 72% at 54°C (Musil et al. 2009). This decline in Rubisco activity preceded by a decrease in PSII electron transport commencing at temperatures much lower than the threshold for Rubisco de-activation, as well as to an increased depletion of succulent leaf water reserves during the dry season through intermittent transpiration to prevent excessive heat accumulation in leaves (Musil et al. 2009). The latter exemplified by the observed restriction of all surviving dwarf succulent populations to the edges of the open-top chambers where greater amounts of fog and dew fall intercepted by the chamber walls provided localised areas of higher



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The 22.4% increase in soil CO2 efflux in response to an average 3.8°C increase in the open top warming chambers measured on the quartz gravel substrates during summer at the study site concurred with a reported 25.8% increase in soil CO2 efflux in response to a similar temperature increase of 4°C in an Alaskan boreal forest (Bergner et al. 2004). However, on the shale, phyllite and limestone derived substrates at the study site a much higher 40.3% increase in soil CO2 efflux was recorded during spring. These increases in soil CO2 effluxes coinciding with intermittent precipitation events, which are known to provide an enormous stimulus to microbial activity resulting from an accumulation of nutrients in the soils during the extensive dry periods. This unique feature of arid regions designates them as sinks for carbon-based compounds during dry periods and sources of atmospheric CO2 during wet periods (Huxman et al. 2004). Nevertheless, the measured soil CO2 effluxes in this study (range: 0.11 to 6.15 g C m-2 d-1) were over 3 times less than those reported for temperate and tropical forest ecosystems (up to 34.3 g C m-2 d-1), though during intermittent wet phases soil respiration rates pulses were up to 15 orders of magnitude greater than those during dry phases but still only comparable in magnitude with those reported for temperate semi-arid grasslands (up to 7.3 g C m-2 d-1).

Conclusions This study’s findings confirm that even mild anthropogenic warming is likely to exceed the thermal thresholds of many southern African lichens and quartz field succulent plants leading to metabolic impairment and increased likelihood of localised extinction. They also concur that arid ecosystem soils are relatively minor sources of CO2 emissions and likely to have a minor impact on atmospheric CO2 with global warming.

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Acknowledgements The authors’ general acknowledgements to the organisations and institutions, which supported this work are provided in Volume 1. References Adachia, M., Bekkub, Y.S., Rashidahc, W., Okudad, T., Koizumie, H. (2006): Differences in soil respiration between different tropical ecosystems. – Applied Ecology 34: 258–265. Amy, T.A., Laura, Y., John M.S., Jayne, B., Amilcare, P., Urszula, N., Damián, A.R., Sean, M.S. (2004): Water pulses and biogeochemical cycles in arid and semiarid ecosystems. – Oecologia 141: 221–235. Bergner, B., Johnstone, J.F., Treseder K.K. (2004): Experimental warming and burn severity alter CO2 flux and soil functional groups in recently burned boreal forest. – Global Change Biology 10: 1996–2004. Golding, A.J., Johnson, G.N. (2003): Down regulation of linear and activation of cyclic electron transport during drought. – Planta 218: 107–114. Herk, C.M. van, Aptroot, A., van Dobben, H.F. (2002): Long-term monitoring in the Netherlands suggests that lichens respond to global warming. – The Lichenologist 34: 41–154. Hilton-Taylor, C. (1996): Patterns and characteristics of the flora of the Succulent Karoo Biome, southern Africa. – In: van der Maesen, L.J.E., van der Burgt, X.M., van Medenbach de Rooy, J.M. (eds.): The biodiversity of African plants: 58–72. Dordrecht: Kluwer Academic Publishers. Hui, D., Luo, Y. (2004): Evaluation of soil CO2 production and transport in Duke Forest using a process-based modelling approach. – Global Biogeochemical Cycles 18: 1–10. Hulme, M., Doherty, R., Ngara, T., New, M., Lister, D. (2001): African climate change: 1900–2100. – Climate Research 17: 145–168. Huxman, T.E., Snyder, K.A., Tissue, D., Laffler, A.J., Ogle, K., Pocman, W.T., Sandquist, D.R., Potts, D.L., Schwinning, S. (2004): Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. – Oecologia 141: 254–268. IPCC (Intergovernmental Panel on Climate Change) (2007): Summary for policy makers. – In: Solmon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor M., Miller, H.L. (eds.): Climate change 2007: the physical science basis. Contributions of working group 1 to the fourth assessment report of the intergovernmental panel on climate change: 1–18. Cambridge: Cambridge University Press. Jia, B., Zhou, G. (2008): Integrated diurnal soil respiration model during growing season of a typical steppe: effects of temperature, soil water content and biomass production. – Soil Biology and Biochemistry 41: 681–686. Kappen, L. (1981): Ecological significance of resistance to high temperatures. – In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (eds): Physiological plant ecology I. Responses to the physical environment. Encyclopedia of Plant Physiology, New Series 12A: 439– 474. Berlin: Springer. Klak, C., Reeves, G., Hedderson, T. (2004): Unmatched tempo of evolution in South African semi-desert ice plants. – Nature 427: 63–65. Lin, G., Ehleringer, J.R., Rygiewicz, P.T., Johnson, M.G., Tingey. D.T. (1999): Elevated CO2 and temperature impacts on different components of soil CO2 efflux in Douglas-fir terracosms. – Global Change Biology 5: 157–168.

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soil moisture conducive for transpiration to cool leaf surfaces (Musil et al. 2009). All four lichen species displayed significantly (p ≤ 0.05) diminished photosynthetic quantum yields, a sensitive indicator of photosystem II efficiency and stress (Golding & Johnson 2003), in response to experimental warming with the greatest reductions (range: 46.8% to 149.2%) also apparent in late autumn 12-months after open top warming chamber placement (Fig. 2). These measured declines in photosynthetic quantum yield in response to experimental warming were generally of much greater magnitude than the reductions in numbers of live leaves measured in the dwarf succulents implying that lichens may provide sensitive indicators of climate change. In fact, a recent study in the Netherlands has identified recent major changes in lichen distribution independent of pollution since 1979. Warm-temperate lichen species have significantly increased, and species characteristic of cold environments have either decreased or disappeared (van Herk et al. 2002). One example is that of Flavoparmelia soredians a drought resistant, warmtemperate lichen species presently common in the Netherlands but rare before 1900 with its northern most limit until recently in southern England (Seaward & Coppins 2004). Substantially higher soil CO2 effluxes were measured in soils with moderate than sparse vegetation cover (Fig. 2), a consequence of the added contribution of root respiration and leaf fall detritus decomposition to total soil respiration (Huxman et al. 2004). In the moderately vegetated soils, approximately 62% of the total soil CO2 efflux was contributed by root respiration, this percentage only slightly higher than the reported 53% contribution by root respiration to total soil CO2 efflux in the Duke forest in USA (Hui & Luo 2004). The experimentally elevated temperatures in the open top warming chambers generally had only small statistically insignificant (p ≥ 0.05) effects on soil CO2 effluxes in the moderately vegetated soils with only two incidences of significantly (p ≤ 0.05) elevated soil CO2 efflux in the sparsely vegetated soils (Fig. 2).

Experiments

Musil, C.F., van Heerden, P.D.R., Cilliers, C.D., Schmiedel, U. (2009): Mild experimental climate warming induces metabolic impairment and massive mortalities in southern African quartz field succulents. – Environmental and Experimental Botany 66: 79–87. Myers, N., Mittermeier, R.A., Mittermeir, C.G., Da Fonseca, G.A.B., Kent, J. (2000): Biodiversity hotspots for conservation priorities. – Nature 403: 853–858. Nobel, P.S. (1989): Shoot temperatures and thermal tolerances for succulent species of Haworthia and Lithops.– Plant, Cell & Environment 12: 643–651. Raich, J.W., Tufekcioglu, A. (2000): Vegetation and soil respiration: Correlations and controls. – Biogeochemistry 48: 71–90.

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Reichstein, M., Rey, A., Freibauer, A., Tenhunen, J., Valentini, R., Banza, J., Casals, P., Cheng, Y., Grünzweig, J.M., Irvine, J., Joffre, R., Law, B.E., Loustau ,D., Miglietta, F., Oechel, W., Ourcival, J.M., Pereira, J.S., Peressotti, A., Ponti, F., Qi, Y., Rambal, S., Rayment, M., Romanya, J., Rossi, F., Tedeschi, V., Tirone, G., Xu, M., Yakir D. (2003): Modelling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices. – Global Biogeochemical Cycles 17(4): Art. No. 1104. Rustad, L.E., Campbell, J.L., Marion, G.M., Norby, R.J., Mitchell, M.J., Hartley, A.E., Cornelissen, J.H.C., Gurevitch, J. (2001): A meta-analysis of the response of soil net nitrogen mineralisation, and aboveground plant growth to experimental ecosystem warming. – Oecologia 126: 543–562.

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Sánchez, M.L., Ozores, M.I., López, M.J., Colle, R., De Torre, B., Garcıá, M.A., Pérez, I. (2003): Soil CO2 fluxes beneath barley on the central Spanish plateau. – Agricultural Forestry and Meteorology 118: 85–95. Schlesinger, W.H., Andrews, J.A. (2000): Soil respiration and the global carbon cycle. – Biogeochemistry 48: 7–20. Schmiedel, U., Jürgens, N. (2004): Habitat ecology of southern African quartz fields: studies on the thermal properties near the ground. – Plant Ecology 170: 153–166. Seaward, M.R.D., Coppins, B.J. (2004): Lichens and hypertrophication. – Bibliotheca Lichenologica 88: 561–572. Zhou, X., Sherry, R.A., An, Y., Wallace, L.L., Luo, Y. (2006): Main and interactive effects of warming, Clipping and doubled precipitation on soil CO2 efflux in a grassland ecosystem. – Global Biogeochemical Cycles 20: GB1003, doi:10.1029/2005GB002526.

