Herbivorous Prairie Insects Can Be Co-Limited by Macronutrients and Sodium

Ecology Letters, (2018) 21: 1467–1476 doi: 10.1111/ele.13127 LETTER Seeking salt: herbivorous prairie insects can be co-limited by macronutrients and sodium Abstract Chelse M. Prather,1,2* The canonical factors typically thought to determine herbivore community structure often explain Angela N. Laws,3,4 only a small fraction of the variation in herbivore abundance and diversity. We tested how Juan F. Cuellar,3,† macronutrients and relatively understudied micronutrients interacted to influence the structure of Ryan W. Reihart,2 insect herbivore (orthopteran) communities. We conducted a factorial fertilisation experiment Kaitlin M. Gawkins2 and manipulating macronutrients (N and P, added together) and micronutrients (Ca, Na and K) in 9 2 Steven C. Pennings3 large plots (30 30 m ) in a Texas coastal prairie. Although no single or combination of micronutrients affected herbivore communities in the absence of additional macronutrients, macronutrients and sodium added together increased herbivore abundance by 60%, richness by 15% and diversity by 20%. These results represent the first large-scale manipulation of single micronutrients and macronutrients in concert, and revealed an herbivore community co-limited by macronutrients and Na. Our work supports an emerging paradigm that Na may be important in limiting herbivore communities. Keywords Acrididae, grassland, micronutrient, nutrient limitation, prairie, sodium, tettigonidae. Ecology Letters (2018) 21: 1467–1476 (Haddad et al. 2001; Joern et al. 2012). However, some of the INTRODUCTION intricacies of these factors have not been fully examined. For An understanding of the factors that determine herbivore instance, most research examining the role of plant nutritional abundance and diversity is of fundamental ecological interest. quality has only considered herbivore limitations by either N It is also necessary for the control of some herbivore species or P; N is a key component of amino acids (and proteins) that cause damage (Hulme 1994; Branson et al. 2006) and to while P is a defining element in nucleic acids and phospho- support those species that are important purveyors of ecosys- lipids. Following others (Kaspari & Powers 2016; Bonoan tem services (McNaughton et al. 1997; Prather et al. 2012). et al. 2018), here we refer to N and P as ‘macronutrients’, and Several canonical factors are typically thought to largely regu- elements that are rarer in living tissues as ‘micronutrients’. In late herbivore communities, including top-down consumers the same way that multi-nutrient studies have shed new (Spiller & Schoener 1990; Dial & Roughgarden 1995) and bot- insight into limitations on plant diversity and abundance tom-up resources, typically characterised as plant biomass (Harpole et al. 2016), experiments that incorporate multiple (Lawton 1983; McNaughton et al. 1989; Lewinsohn et al. nutrients to examine the possibility of multiple resource limi- 2005; Wimp et al. 2010), plant diversity (Hutchinson 1959; tation (co-limitation) or that manipulate micronutrients may May 1990; Siemann et al. 1998; Pakeman & Stockan 2014), provide a better understanding of the relative importance of and plant nutritional quality (White 1984; Fagan et al. 2002; the factors that structure herbivore communities. Huberty & Denno 2006; Joern et al. 2012). Although manipu- The historical focus on single factor limitation arose lations of any one these factors has usually resulted in some through the application of a parsimonious and logical con- change to herbivore communities, our ability to explain herbi- cept: Leibig’s law of the minimum (van der Ploeg & Kirkham vore abundance and diversity is still relatively weak. For 1999). This law posits that one resource limits a population of example, plant richness only explains ~ 20% of the variation organisms at any given time, and that the limiting resource is in herbivore richness across 320 studies (Castagneyrol & Jactel that which has the highest demand to supply ratio (but see 2012). Similarly, other single factors like top-down consumers, Wilder & Eubanks 2010). For example, in the case of single plant productivity, and plant nutritional quality (often mea- nutrient limitation, the nutrient with the highest ratio of con- sured as the stoichiometry of nitrogen, N, and phosphorus, P) centration in an organism’s body compared to the concentra- clearly influence herbivore communities, but considerable vari- tion of the nutrient in the organism’s food would be assumed ation remains unexplained (e.g. Letourneau et al. 2009), even to be the single limiting nutrient in that ecosystem. Nutrient when more than one of these factors are considered together limitation of herbivores, in particular, has largely focused on 1Department of Biology, Radford University, Radford, VA 46556, USA †Present address: Department of Surgical Pathology, Northwestern University, 2Department of Biology, University of Dayton, Dayton, OH 45469, USA 251 E. Huron, Galter 7-281A, Chicago, IL 60611, USA 3Department of Biology and Biochemistry, University of Houston, Houston, *Correspondence and present address: Chelse M. Prather, Department of TX 77204, USA Biology, University of Dayton, Dayton, OH 45469, USA 4The Xerces Society, Sacramento, CA 95814, USA E-mail: [email protected] © 2018 John Wiley & Sons Ltd/CNRS 1468 C. M. Prather et al. Letter single nutrient limitation, with first a focus on nitrogen (Matt- membranes (e.g. the sodium pump); generating electrical son 1980; White 1984), and later on phosphorus (Urabe & impulses in excitable cells, like neurons, via sodium channels; Watanabe 1992; DeMott et al. 1998; Sterner & Schulz 1998), maintaining hydrologic homeostasis; and supporting neural especially in cases when N was abundant (Elser et al. 2001; and brain development (Snell-Rood et al. 2014). Na may also Makino et al. 2002; Huberty & Denno 2006; Tao & Hunter be important for reproduction in orthopterans, as suggested 2012). This focus on N and P was logical: both have relatively by changes in nymphal Na concentrations: newly hatched high demand to supply ratios in herbivores with much higher nymphs have the highest Na which steadily decreases over N and P concentrations in herbivore body tissues than plants their development (Boswell et al. 2008). However, with a few (Sterner et al. 1992). exceptions (Beanland et al. 2003; Kaspari et al. 2008, 2010, Plant nutrients, however, have complementary functions 2014, 2017), studies showing the potential importance of whereby some basic physiological function relies on more than micronutrients in animal communities have been correlative one resource being at critical thresholds simultaneously; too or laboratory experiments, and as such, are open to criticisms little of any one of these complementary nutritional resources that they simply reflect unmeasured variables or do not reflect impacts physiological functioning, in particular the mainte- natural conditions. nance of cell and tissue homeostasis. For this reason, the We tested the overarching idea that micronutrients would applicability of Leibig’s law of the minimum to populations alter the abundance and community structure of herbivores and communities has been questioned (e.g. Danger et al. (orthopterans) using a factorial field experiment in a Texas 2008), and now multiple resource limitation is generally recog- prairie with large plots (30 9 30 m2). We chose to focus on nised to likely be common in plant communities (Harpole orthopterans because they are relatively large (for insects), et al. 2011, 2017; Fay et al. 2015). Co-limitation may occur ecologically and economically important, generalist herbivores via several different pathways (Sperfeld et al. 2016): indepen- that are relatively easy to identify to genus or species. We first dent co-limitation occurs when two different nutrients sepa- determined how well orthopteran communities at our site rately enhance populations, and these effects are further were predicted by the canonical variables described above vs. enhanced when both nutrients are abundant: simultaneous relatively understudied plant and soil micronutrients, using an limitation occurs when neither nutrient positively affects an observational approach. Based on these results, we then chose organism, but together they produce a positive effect when a three micronutrients to manipulate (Ca, K and Na) that have critical threshold of both is reached; and serial co-limitation been implicated in structuring insect (Kaspari et al. 2017) and occurs when one of the nutrients produces a moderately posi- orthopteran (Joern et al. 2012) communities in other studies. tive effect that is enhanced by the addition of some other lim- We then tested the hypotheses that micronutrients affect the iting nutrient. Many different reasons may exist for these abundance, diversity, and composition of common grassland different types of co-limitation in consumer communities. For insect herbivores (orthopterans), and that these effects depend instance, Kaspari et al. (2017) suggest serial limitation of on the availability of macronutrients (i.e. that micronutrients insects by macronutrients and Na at their Oklahoma grass- and macronutrients are co-limiting). We measured nutrient land site occurred because macronutrients limited plant bio- effects on plant biomass and chemistry, and also conducted mass whereas both N and Na altered leaf nutritional quality. feeding trials to determine if observed effects were due to Mounting evidence suggests that nutrient co-limitation may changes

Load more