In many ecosystems, seasonal shifts in temperature and precipitation induce pulses of primary productivity that vary in phenology, abundance and nutritional quality. Variation in these resource pulses could strongly influence community composition and ecosystem function, because these pervasive bottom-up forces play a primary role in determining the biomass, life cycles and interactions of organisms across trophic levels. The focus of this research is to understand how consumers across trophic levels alter resource use and assimilation over seasonal and inter-annual timescales in response to climatically driven changes in pulses of primary productivity. We measured the carbon isotope ratios (d13C) of plant, arthropod, and lizard tissues in the northern Chihuahuan Desert to quantify the relative importance of primary production from plants using C3 and C4 photosynthesis for consumers. Summer monsoonal rains on the Sevilleta LTER in New Mexico support a pulse of C4 plant production that have tissue d13C values distinct from C3 plants. During a year when precipitation patterns were relatively normal, d13C measurements showed that consumers used and assimilated significantly more C4 derived carbon over the course of a summer; tracking the seasonal increase in abundance of C4 plants. In the following spring, after a failure in winter precipitation and the associated failure of spring C3 plant growth, consumers showed elevated assimilation of C4 derived carbon relative to a normal rainfall regime. These findings provide insight into how climate, pulsed resources and temporal trophic dynamics may interact to shape semi-arid grasslands such as the Chihuahuan Desert in the present and future.
This research was conducted on the Sevilleta LTER, located 100 km south of Albuquerque, New Mexico, which is an ecotonal landscape of Chihuahuan desert shrub and grasslands (Muldavin et al. 2008). Data were collected from a 0.9 x 0.5km strip of land that encompassed a flat bajada and a shallow rocky canyon of mixed desert shrub and grassland dominated by the creosote bush (Larrea tridentata) and black grama grass (Bouteloua eriopoda).
Tissue collection & sample preparation for stable isotope analysis:
From May to October of 2005 and 2006 we collected plant, lizard, and arthropod tissues for carbon stable isotope analysis. During mid-summer of 2005, we randomly collected leaf and stem samples from the 38 most abundant species of plants; these species produce over 90% of the annual biomass on our study site (see Appendix Table A). Approximately 3.5 mg of plant material was then loaded into pre-cleaned tin capsules for isotope analysis.
All animal research was conducted with the approval of the institutional animal care and use committee (UNM-IACUC #05MCC004). Lizards were captured by hand using noose poles and by drift fence and pitfall trap arrays (Enge 2001) randomly scattered over a 0.5 km2 area. Each lizard was toe clipped for permanent identification and snout-vent length (SVL), body mass (g) and sex were recorded. For stable isotope analysis, we obtained a 50 μL blood sample from each lizard and only sampled individuals once in a two week period. We acquired a total of 367 blood samples from 11 lizard species. Blood samples were obtained by slipping a micro-capillary tube (Fisherbrand heparinized 50μL capillary tubes) ventral and posterior to the eyeball to puncture the retro-orbital sinus. Before and after this procedure a local anesthesia (0.5% tetracaine hydrochloride ophthalmic solution, Akorn Inc.) was applied to the eye. Blood samples were stored on ice and centrifuged within 24 hours to separate plasma and red blood cells. For isotope analysis 15 μL of plasma were pipetted into a tin capsule, air dried, and then folded.
Arthropods were captured bi-weekly from May through October of each year in pitfall traps (see above), as well as by hand and sweep netting. Individuals were frozen, lyophilized, ground into a fine powder and 0.5 mg samples were loaded into tin capsules for isotope analysis.
Stable isotope analysis:
Carbon isotope ratios of samples were measured on a continuous flow isotope ratio mass spectrometer (Thermo-Finnigan IRMS Delta Plus) with samples combusted in a Costech ECS 4010 Elemental Analyzer in the UNM Earth and Planetary Sciences Mass Spectrometry lab. The precision of these analyses was ± 0.1‰ SD for δ13C. A laboratory standard calibrated against international standards (valine δ13C -26.3‰ VPDB [Vienna Pee Dee Belemnite Standard]) was included on each run in order to make corrections to raw values. Stable isotope ratios are expressed using standard delta notation (δ) in parts per thousand (‰) as: δX = (Rsample /Rstandard – 1) x 1000, where Rsample and Rstandard are the molar ratios of 13C/12C of a sample and standard.
Estimation of C3 and C4 carbon incorporation into arthropods and lizards:
We used d13C values of consumer tissues and a two-end-point mixing model to estimate the proportion of a consumer’s assimilated carbon that was derived from each plant photosynthetic type (Martinez del Rio and Wolf 2005):
In this model p is the fraction of dietary C4 plant material incorporated into a sampled tissue. We chose to analyze the isotope composition of whole bodies for arthropods because this best reflects the diet of lizards. For lizards we chose plasma because it has a rapid 13C turnover rate with an inter-specific retention time ranging from 25 to 44 days (Warne et al. 2009b). In the above model Δ is a discrimination factor, which is defined as the difference in isotope values between an animal’s tissues and food when feeding on an isotopically pure diet (DeNiro and Epstein 1978). For our mixing model estimates we used discrimination (Δ13C) values resulting from a diet switch study for two species of lizards (Sceloporus undulatus, and Crotaphytus collaris) fed a diet of C4 raised crickets (Warne et al. 2009b). We found the plasma of these lizards had a mean Δ13C = -0.2 ± 0.4‰ VPDB, while crickets fed a C4 based dog food had a Δ13C = -0.9 ± 0.4‰. Reviews of stable isotope ecology have reported Δ13C values for arthropods ranging from -0.5 ± 0.3‰ (Spence and Rosenheim 2005) to 0.3 ± 0.1‰ (McCutchan et al. 2003). Although variation in our assumed Δ13C values would affect proportional estimates of the C3 or C4 resources consumed, the observed trends would not change.
To compare the seasonal isotope values of consumers between a spring C3 dominated and a summer C4 dominated ecosystem we present the mean δ13C (± SE) of each consumer species during the pre-monsoon (May, June and early-mid-July) and monsoonal periods for each year of this study. We defined the monsoon period to begin with the first day of recorded monsoon rains in July (monsoon 2005 = July 25 to October 15; monsoon 2006 = July 6 to October 15). The effects of seasonal and inter-annual primary production patterns on consumer resource assimilation (δ13C) were determined by two-way ANOVA using the PROC MIXED procedure (Littell et al. 2006) in SAS (SAS 1999). To examine these effects in the lizard community as a whole, lizard species were treated as random effects in the PROC MIXED model. In order to determine the significance of seasonal and year effects post-hoc analyses were conducted using Tukey-Kramer’s hsd test (Sokal and Rohlf 1995). Prior to analysis the data were tested for homogeneity of variance and confirmed to meet the assumptions of ANOVA.