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Stable Isotope Analysis of Diet Confirms Niche Separation of Two 7 8 8 9 Sympatric Species of Namib Desert Lizard 9 10 10 11 11 12 12 13 Ian W

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Stable Isotope Analysis of Diet Confirms Niche Separation of Two 7 8 8 9 Sympatric Species of Namib Desert Lizard 9 10 10 11 11 12 12 13 Ian W Integrative Zoology 2016; 11: 60–75 doi: 10.1111/1749-4877.12170 1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 6 7 Stable isotope analysis of diet confirms niche separation of two 7 8 8 9 sympatric species of Namib Desert lizard 9 10 10 11 11 12 12 13 Ian W. MURRAY,1,* Hilary M. LEASE,1,2 Robyn S. HETEM,1 Duncan MITCHELL,1 Andrea 13 14 14 1 3,4 15 FULLER and Stephan WOODBORNE 15 16 1Brain Function Research Group, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, 16 17 South Africa, 2Biology Department, Whitman College, Walla Walla, Washington, USA, 3iThemba Laboratories, Gauteng, South 17 18 18 Africa and 4Stable Isotope Laboratory, Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, 19 19 Pretoria, South Africa 20 20 21 21 22 22 23 23 24 Abstract 24 25 25 26 We used stable isotopes of carbon and nitrogen to study the trophic niche of two species of insectivorous 26 27 lizards, the Husab sand lizard Pedioplanis husabensis and Bradfield’s Namib day gecko living sympatrically 27 13 15 28 in the Namib Desert. We measured the δ C and δ N ratios in lizard blood tissues with different turnover times 28 29 (whole blood, red blood cells and plasma) to investigate lizard diet in different seasons. We also measured the 29 13 15 30 δ C and δ N ratios in available arthropod prey and plant tissues on the site, to identify the avenues of nutrient 30 31 movement between lizards and their prey. Through the use of stable isotope mixing models, we found that the 31 32 two lizard species relied on a largely non-overlapping but seasonally variable array of arthropods: P. husabensis 32 33 primarily fed on termites, beetles and wasps, while R. bradfieldi fed mainly on ants, wasps and hemipterans. 33 34 Nutrients originating from C3 plants were proportionally higher for R. bradfieldi than for P. husabensis during 34 35 autumn and late autumn/early winter, although not summer. Contrary to the few available data estimating the 35 36 trophic transfer of nutrients in ectotherms in mixed C3 and C4/crassulacean acid metabolism (CAM) plant 36 37 landscapes, we found that our lizard species primarily acquired nutrients that originated from C4/CAM plants. 37 38 This work adds an important dimension to the general lack of studies using stable isotope analyses to estimate 38 39 lizard niche partitioning and resource use. 39 40 40 41 Key words: Namib Desert, niche partitioning, Pedioplanis, Rhoptropus, stable isotopes 41 42 42 43 43 44 44 45 45 Correspondence: Ian W. Murray, Brain Function Research 46 INTRODUCTION 46 Group, School of Physiology, Faculty of Health Sciences, 47 47 For all species there exists a particular set of biotic 48 University of the Witwatersrand, Johannesburg, South Africa. 48 and abiotic conditions that bound their existence, which 49 Email: [email protected] 49 may be thought of as the species’ niche (Hutchinson 50 Present address: Pima County Office of Sustainability and 50 1957). Species niches can be characterized by habitat 51 Conservation, Tucson, AZ 85701, USA. 51 60 © 2015 International Society of Zoological Sciences, Institute of Zoology/ Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd Stable isotope niche of Namib Desert lizards 1 requirements, geographical distribution, thermal niches δ15N may be used as an indication of an organism’s 1 2 or other dimensions, which may not be independent of trophic level (DeNiro & Epstein 1981; Peterson & 2 3 each other. Resource use is one niche dimension that is Fry 1987). Conversely, tissue δ13C changes very little 3 4 widely studied because the resources that organisms use (approximately 0–1.0‰), on average, across trophic 4 5 play an important role in determining species diversity, levels within a food web; consequently, δ13C may 5 6 and may allow different species within a similar feeding be used to trace carbon sources (DeNiro & Epstein 6 7 guild to coexist in the same habitat (Simberloff & 1978; Peterson & Fry 1987). During photosynthesis 7 8 Dayan 1991). Within the same feeding guild, a species plants discriminate against carbon dioxide molecules 8 9 may be a resource specialist or a resource generalist containing the 13C isotope. However, due to differences 9 10 (Futuyma & Moreno 1988). Habitats usually will be in the enzymes responsible for carboxylation, plants 10 11 able to support a greater number of specialist species which use the C3 photosynthetic pathway (e.g. trees 11 12 that consume non-overlapping resources than generalist and most forbs) have significantly lower 13C values 12 13 species that overlap in their resource consumption compared to plants that use either the C4 (e.g. many 13 14 (Roughgarden 1974). This is due to competitive grasses) or crassulacean acid metabolism (CAM; many 14 15 exclusion, the theory that two similar species are unable succulents) photosynthetic pathway. These differences 15 13 16 to coexist with one another unless there is some level lead to C3 plants having a lower δ C ratio compared 16 17 of divergence in how they use resources (Hardin 1960; to C4/CAM plants (Ehleringer et al. 1986, 1997). C3 17 18 Pianka 1974). Indeed, a basic premise of community and C4/CAM plants also have important structural 18 19 ecology is that the coexistence of otherwise similar differences (e.g. C4 plants are characterized by Kranz 19 20 species within a feeding guild may be accomplished by anatomy, which includes the presence of thick-walled 20 21 the use of distinct resources (MacArthur 1958; Bowers bundle sheath cells), which influence their nutritional 21 22 & Brown 1982). profitability to consumers, and may have distinct 22 23 Research on lizard community structure and function growth responses to seasonal patterns of precipitation 23 24 has been important for characterizing the concept of the and climate (Ode et al. 1980; Schulze et al. 1996; 24 25 species niche, as well as understanding how different Barbehenn et al. 2004a,b; Muldavin et al. 2008). 25 26 species coexist (e.g., Schoener 1977; Pianka 1986). Arid Consequently, ecosystem primary productivity can be 26 27 ecosystems in particular may be ideal places to examine divided into distinct resource compartments based on 27 28 species niche partitioning because in such environments plant photosynthetic pathways. 28 29 lizard diversity is often high, it can be relatively easy Importantly, the physiological differences between 29 30 30 to secure large samples of individual lizards (Pianka C3 and C4/CAM plants mean that they are likely to be 31 1986), and limited resources have the potential to affected differently under current projections of climate 31 32 32 intensify competition (MacArthur & Levins 1967). For change and enhanced atmospheric CO2 levels (IPCC 33 33 example, despite the low availability of plant resources, 2014). For example, higher CO2 levels may improve 34 34 the Namib Desert is home to a diverse lizard fauna with C3 plant nutrient and water use efficiency, and favor 35 high levels of endemism (Robinson & Cunningham plants with high demands for woody structural tissue, 35 36 1978; Murray & Schramm 1987; Herrmann & Branch such as trees, compared to herbaceous plants, such as 36 37 37 2013), and, as with other hot deserts, high lizard grasses (most of which are C4 in arid regions; Drake et 38 biomass may represent an important component of the al. 1997; Bond et al. 2003). However, warmer and drier 38 39 39 food web in this ecosystem (Pianka 1986). However, climatic conditions would tend to favor C4/CAM plants 40 few studies to date have examined resource partitioning (Bond et al. 2003). From a consumer’s perspective 40 41 and trophic dynamics within the Namib lizard fauna these differences matter because many animals 41 42 42 (Robinson & Cunningham 1978; Murray & Schramm selectively forage on either C3 or C4/CAM plants, and 43 1987; Murray et al. 2016). the nutritional quality of these plant groups is not the 43 44 13 44 The use of stable isotopes, particularly carbon (δ C) same (Ehleringer et al. 2002; Barbehenn et al. 2004a,b). 45 15 45 and nitrogen (δ N) stable isotopes, is an effective and Furthermore, enhanced CO2 levels may translate into 46 46 minimally invasive way to quantify the spatial and negative consumer effects due to lower plant tissue 47 47 temporal patterns of consumer resource partitioning nitrogen content and higher carbon to nitrogen ratios 48 48 (Gannes et al. 1997; Boecklen et al. 2011). Because (Ehleringer et al. 2002). 49 49 tissue δ15N increases by approximately 3.0‰, on Here we investigate and compare the resource 50 50 average, across each trophic level within a food web, partitioning of 2 sympatric and similarly-sized species 51 51 © 2015 International Society of Zoological Sciences, Institute of Zoology/ 61 Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd I. W. Murray et al. 1 of insectivorous Namib lizards. The Husab sand lizard, Lizard tissue collection 1 2 Pedioplanis husabensis Berger-Dell’Mour & Mayer, 2 3 1989, is a 2.5–3.0-g lacertid lizard endemic to rocky We captured lizards during austral summer 3 4 substrates in the west-central Namib Desert between the (December 2012–January 2013) and austral autumn 4 5 ephemeral Swakop and Khan Rivers (Berger-Dell’Mour (May 2013) using noose poles. We took blood samples 5 6 & Mayer 1989). Bradfield’s Namib day gecko, (approximately 50 µL) from the infraorbital sinus with 6 7 Rhoptropus bradfieldi Hewitt, 1935, is a 3.0–4.0-g rock- heparinized capillary tubes before releasing the lizards 7 8 dwelling diurnal gecko endemic to the Namib Desert unharmed (Murray et al.
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