Editor’s Choice @Biotropica 48(2): Tracking Nutrients in Avian Consumers in a Subtropical Desert
I am pleased to announce the Editor’s Choice Article for Biotropica 48(2): Herrera M., L. G. and Osorio M., J. (2016), Tracking Nutrient Routing in Avian Consumers in a Subtropical Desert. Biotropica, 48(2): 255–264.
Stable isotopes are a tool with a storied history in ecology. In this issue’s Editor’s Choice article, Herrera and colleagues used them to bring together two questions central to understanding the ecology and evolution of biodiversity in tropical ecosystems — how and where do animals get the nutrients required to grow and survive? These important questions, and the rigorous approach to addressing them, were obviously central to the study’s selection as the EC article. However, we also wanted to highlight the important role physiological ecology has played in our understanding of tropical biota, as well as the fact that the tropics are more than lowland forests – they also include the arid ecosystems such as the Tehuacán-Cuicatlán Valley that are both biologically fascinating and increasingly threatened. And of course, any study in which the researchers collect breath samples from over 45 species of birds…that’s right, breath samples from birds. Read more below in the essay by Dr. Herrera, and thanks to the authors for choosing Biotropica as the outlet for this fascinating study.
Animals must obtain an array of macronutrients while foraging to sustain different physiological functions. Tracking how animals allocate the nutrients that they ingest is not an easy task, but it has being facilitated by the incorporation of stable isotope analysis (SIA) to the toolbox of animal ecologist and physiologist. The use of SIA to trace food webs is based on the existence of contrasting isotopic ratios in available food sources that are then transferred to the consumer tissues. Isotopic ratios are expressed as a parts-per-thousand difference in the ratio of the heavier (more rare) to the lighter (more common) isotope, compared with the ratio found in an international standard. A handful of studies have used the SIA approach to test if animals use the same kind of macronutrients to sustain oxidative metabolism and to build tissue. These two functions are fundamental for organism’s survival yet there is little information of how wild animals allocate macronutrients to fulfill them. The utility of the SIA to resolve this issue depends primarily on how isotopically different are food sources serving dissimilar nutritional roles. An ideal scenario to unveil how food resources are used is provided by the isotopic mosaic of terrestrial dry ecosystems. For this reason, we chose the Tehuacán-Cuicatlán Valley several years ago to follow the path of nutrients into the animal community.
The Tehuacán-Cuicatlán Valley is a subtropical semiarid ecosystem in Central Mexico considered as the center of diversification of cactus and agaves. Every year, the valley thrives with the surplus of flowers and fruits that these plants produce and that potentially benefit the animal community in the form of nectar, pollen, pulp, and seeds. The valley has been of interest to naturalists and ecologists that have documented over several decades the use of these plants by all sorts of animals, including birds, bats, reptiles and insects. In the last decade, tracking how cactus and agave food resources flow into the animal community has benefited by the implementation of SIA. Cactus and agaves use the Crassulacean acid metabolism (CAM) for photosynthesis, a mechanism that has evolved in some plants as an adaptation to arid conditions. In contrast, most terrestrial plants use the Calvin-Benson cycle path way (C3 photosynthesis). Due to contrasting discrimination processes that favor the use of the lighter carbon isotope (12C) during photosynthesis, tissues of CAM plants are richer in the heavier isotope (13C) than C3 plants. This particularity forms an isotopic collage in terrestrial ecosystems where both CAM and C3 plants coexist, such as the Tehuacán-Cuicatlán Valley. We have been tracking feeding habits in bats and birds in this area in the last few years and we noticed that although SIA of tissues in some species indicates no contribution of CAM plants, examination of fecal remains indicates otherwise. We hypothesized that contribution of CAM plants in these species might be in the form of energy to sustain oxidative metabolism. For example, insectivorous birds might be using protein derived from C3 insects to build tissues, but use carbohydrates from CAM fruits to meet energy demands.
We collected breath and feathers from 5 species of hummingbirds, and breath, plasma and red blood cells from 47 bird species representing frugivorous, granivorous and insectivorous guilds. To collect breath samples, my graduate student Jazmín Osorio placed each individual in a 1-L plastic container connected to a portable air pump which injected air filtered through a Drierite-Ascarite column to scrub CO2 and residual water. After a few minutes, the container was sealed and each bird was left breathing inside the container to allow the accumulation of breath CO2. Jazmín released birds after rewarding them with a sugary solution for their cooperation. We assumed that carbon SIA of breath represents oxidative metabolism, whereas SIA of feather, plasma and red cells represent tissue building. We expected that the importance of CAM-derived food (RCCAM) in frugivores and granivores was similar to fuel oxidative metabolism and for tissue building, that RCCAM in nectarivores was highly important to fuel metabolism but of low importance to generate tissues, and that (although low) RCCAM in insectivores was higher to sustain metabolism than to build tissues. We also examined selected populations and individuals within each guild. RCCAM was high for oxidative metabolism but low for feather production in nectarivores, intermediate for oxidative metabolism and low to build tissues in frugivores, intermediate for both oxidative metabolism and tissue building in granivores, and low for oxidative metabolism and intermediate for tissue building in insectivores. Our examination at trophic guild, population and individual levels showed that in general nutrients used to sustain oxidative metabolism and tissue construction had a uniform isotopic origin, suggesting that the avian community studied is not characterized by routing different food groups to fulfill different needs. However, we found exceptions to this general pattern that warrants further application of the SIA approach to disentangle how animals use different types of food in dry ecosystems. Our study, along with previous work we have conducted in the study site, confirms that nutrients derived from columnar cactus and agaves do not cascade equally into all members of the vertebrate community and that its importance might be limited to some functional groups. Given the large extension of cactus and agave land in Mexico, we hope that our work stimulates other colleagues and students to use SIA to track how these ecosystems function.