IPBRG Investigators:  Spence Behmer, Andy Boswell, Steve Cook, Marion Le Gall, Karl Roeder
 

Collaborators:  Roger Gold (TAMU), Micky Eubanks (TAMU), Tony Joern (KSU),
                         David Raubeheimer (Auckland, NZ), Steve Simpson (Sydney, AUS),
                         Andrew Smith (Oxford, UK), Tony Zera (UNL)

Two key ideas drive this area of research. First, physiological mechanisms can provide unique insights into ecological patterns and processes. Second, animal behavior provides a window through which physiology can be viewed. Much of what we do under the remit of physiological ecology centers on nutritional physiology and the mechanisms associated with resource use. Additionally, where possible, we use a comparative approach to gain insights into the evolution of physiological processes and mechanisms.

Knowing how insects use available resources provides the foundation for understanding a variety of issues, ranging from individual behavior up to population and community level processes. Over the past few years we have been exploring resource use in herbivorous insects with the aid of a recently developed experimental approach, called the 'Geometric Framework' (GF), which emphasizes nutrient regulation. The GF is unique in that it allows for clear descriptions to be made of the foraging compromises and tradeoffs insect herbivores make when confronted with foods that vary nutritionally, contain defensive compounds and/or are variously distributed in the environment. We also use the experimental approach of the GF to study post-ingestive physiological processes. For example, by measuring body nitrogen and lipid content, we are able to examine issues related to resource utilization efficiency. Locusts, grasshoppers and caterpillars are our primary study organisms, but recently we have extended our investigations to ants.

Results from experiments using locusts (e.g. Locusta migratoria, shown on the right) and caterpillars show that insect herbivores are very responsive to the type and distribution of foods in their environment, and that they tightly regulate their macronutrient intake with respect to changes in the relative frequency at which nutritionally distinct foods occur in the environment (Behmer et al. 2001), and across different spatial distances (van der Zee et al. 2002, Behmer et al. 2003). This data demonstrates that nutrient regulation is not a passive process, and behavioral observations have allowed us to identify the regulatory mechanisms that are being used. For example, locusts respond to changes in the relative frequency of foods by increasing their preference and fidelity to rare food types. As the distance between foods increases, they display a propensity to stay near rare foods and decrease the number of visits to other foods.

We have also studied, within a nutritional context, how the interplay between plant nutrients and allelochemicals affects insect herbivores. Our work shows that the extent to which herbivores ingest defensive compounds depends on the nature of the compound (whether it is carbon- or nitrogen-based), as well as the nutrient content (protein-carbohydrate ratio) of available foods (Behmer et al. 2002; Behmer et al. in prep). Additionally, our work suggests that the deterrent effect of a C-containing defensive compound (e.g. tannic acid) increases as protein content decreases, but that the opposite appears to be true for a N-containing defensive compound (e.g. gramine). A particularly novel finding is that tolerance towards toxic and deleterious compounds increases as nutrient intake approaches optimal levels. Combined, these results are helping to clarify various plant-defense theories.

We have also investigated the extent to which physiological processes and traits associated with resource use in plant-feeding insects can evolve and are heritable. Here diamondback moth (Plutella xylostella) larvae were reared for multiple generations in a quasi-natural selection experiment on Arabidopsis starch mutants or chemically defined synthetic foods with fixed nutritional differences (Warbrick-Smith et al. 2006). Results from these experiments indicate that plant macronutrient content interacts with patterns of nutritional heterogeneity in the environment to influence the evolution and expression of physiological and behavioral traits, including ovipositional preferences.

At the present we are investigating, via an NSF grant (DEB section in Ecology), whether physiological mechanisms can shed light on ecological patterns (Tony Joern, shown to the right, is the co-PI). How multiple species coexist within a single habitat is a question that has long interested entomologists and ecologists, and we are interested in the idea that species coexist by occupying unique nutrient-based feeding niches. Our project, which uses grasshopper assemblages found in the sandhills of western Nebraska, aims to identify and explore the link between physiological and ecological factors that explain species coexistence, and that drive fluctuations in the relative abundance of generalist-feeding insect herbivores. Initial results from this project have just been published in PNAS (Behmer & Joern 2008).

Finally, we are interested in the physiological adaptations herbivores employ for dealing with plants that contain heavy metals (Behmer et al. 2005). Plants that hyperaccumulate heavy metals have drawn interest for their phytoremediation potential, but they are also interesting in that they might be involved in mediating biotic interactions with plant-feeding insects, in a manner analogous to plant-produced allelochemicals. Additionally, because heavy-metal hyperaccumulation is a recent phenomenon in plants, interesting evolutionary questions pertaining to host use can be asked.

Key Publications:

Behmer, S.T. (2009) Insect herbivore nutrient regulation. Annual Review of
     Entomology 54, 165-187. (click here for a free PDF)

Behmer, S.T. (2009) Animal behaviour: feeding the superorganism. Current Biology 19,

     R366-R368. [pdf]

Warbrick-Smith, J., Simpson, S.J. Raubenheimer, D. and Behmer, S.T. (2009). Three hundred
     and fifty generations of extreme food specialization: testing a prediction of nutritional
     ecology. Entomologia Experimentalis et Applicata 132, 65-75. [pdf]

Behmer, S.T. and Joern, A. (2008) Coexisting generalist herbivores occupy unique
     nutritional feeding niches. Proceedings of the National Academy of Sciences,
     USA 105, 1977-1982 [pdf].

Boswell, A.W., Provin, T. and Behmer, S.T. (2008) The relationship between body mass and
     elemental composition in nymphs of the grasshopper Schistocerca americana. Journal
     of Orthoptra Research 17, 1-7. [pdf]

Warbrick-Smith, J., Behmer, S.T., Lee, K.P., Raubenheimer, D. and Simpson, S.J. (2006)
     Evolving resistance to obesity in an insect. Proceedings of the National Academy of
     Sciences, USA 103, 14045-14049. [pdf]

Lee, K.W., Behmer, S.T. and Simpson, S.J. (2006) Nutrient regulation in relation to diet
     breadth: a comparison of Heliothis sister species and a hybrid. Journal of Experimental
     Biology 209, 2076-2084. [pdf]

Behmer, S.T., Lloyd, C.M., Raubenheimer, D., Stewart-Clark, J., Knight, J., Leighton, R.S.,
     Harris, F.A. and Smith, J.A.C. (2005) Metal hyperaccumulation in plants: mechanisms of
     defence against insect herbivores. Functional Ecology 19, 55-66. [pdf]

Simpson, S.J., Sibly, R.M., Lee, K., Behmer, S.T. and Raubenheimer, D. (2004) Optimal foraging
     with multiple nutrient requirements. Animal Behaviour 68, 1299-1311. [pdf]

Opstad, R., Rogers, S.M., Behmer, S.T. and Simpson, S.J. (2004) Behavioural correlates
     of phenotypic plasticity in mouthpart chemoreceptor numbers in locusts. Journal of
     Insect Physiology 50, 725-736. [pdf]

Behmer, S.T., Raubenheimer, D. and Simpson, S.J. (2003) The effects of distance between
     foods on nutrient regulation in a highly mobile insect herbivore.
     Animal Behaviour 66, 665-675. [pdf]

Lee, K.P., Raubenheimer, D, Behmer, S.T. and Simpson, S.J. (2003) A correlation between
     macronutrient balancing and insect host-plant range: evidence from the specialist caterpillar
     Spodoptera exempta (Walker). Journal of Insect Physiology 49, 1161-1171. [pdf]

Behmer, S.T., Simpson, S.J. and Raubenheimer, D. (2002) Herbivore foraging in chemically
     heterogeneous environments: nutrients and secondary metabolites.
     Ecology 83, 2489-2501. [pdf]

van der Zee, B., Behmer, S.T. and Simpson, S.J. (2002) Food mixing strategies in the
     desert locust:effects of phase, distance between foods and food nutrient content.
     Entomologia Experimentalis et Applicata 103, 227-237. [pdf]

Lee, K.W., Behmer, S.T., Raubenheimer, D. and Simpson, S.J. (2002) A geometric analysis of
     nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of
     Insect Physiology 48, 655-665. [pdf]

Simpson, S.J., Raubenheimer, D., Behmer, S.T., Whitworth, A. and Wright, G.A. (2002)
     A comparison of nutritional regulation in solitarious and gregarious phase nymphs
     of the desert locust, Schistocerca gregaria. Journal of Experimental Biology 205,
     121-129. [pdf]

Behmer, S.T., Raubenheimer, D. and Simpson, S.J. (2001) Frequency-dependent food
     selection in locusts:a geometric analysis of the role of nutrient balancing. Animal
     Behaviour 61, 995-1005. [pdf]

Frazier, M.R., Harrison, J.F. and Behmer, S.T. (2000) Effects of diet on titratable acid-base
     excretion in grasshoppers. Physiological and Biochemical Zoology 73, 66-76. [pdf]

Joern, A. and Behmer, S.T. (1998) Impact of diet quality on demographic attributes in adult
     grasshoppers and the nitrogen limitation hypothesis. Ecological Entomology 23,
     174-184. [pdf]

Joern, A. and Behmer, S.T. (1997) Importance of dietary nitrogen and carbohydrates to survival,
     growth and reproduction in adults of the grasshopper Ageneotettix deorum
     (Orthoptera: Acrididae). Oecologia 112, 201-208. [pdf]

Chambers, P., Sword, G., Angel, J., Behmer, S. and Bernays, E.A. (1996) Foraging by
     generalist grasshoppers: dietary mixing and the role of crypsis.
     Animal Behaviour 52, 155-165. [pdf]

Behmer, S. and Joern, A. (1994) The influence of proline on diet selection: sex-specific feeding
     preferences by the grasshoppers Ageneotettix deorum and Phoetaliotes nebrascensis
     (Orthoptera: Acrididae). Oecologia 98, 76-82. [pdf]

Behmer, S. and Joern, A. (1993) Diet choice by a grass-feeding grasshopper based on the need
     for a limiting nutrient. Functional Ecology 7, 522-527. [pdf]