Nutritional ecology, functional ecology and Functional Ecology

Abstract

‘Nutritional ecology’ is a bit like ‘art’: easy to recognize but difficult to define. We believe that this is, in part, because the field has progressed on a broad (even diffuse) front, and has lacked cohesion or commonality of purpose. Our aim in this special feature is to bring together leading researchers drawn from across this spectrum and have them review what they consider to be the key issues in their respective research areas. The mandate for invited authors was broad, with invitations that were no more specific than: ‘contribute a paper that provides an overview of the achievements, opportunities and limitations of nutritional ecology studies of [respective taxon/thematic research area]’. The special feature, we hope, will provide a lens that focuses attention on similarities and highlights disparities across the field. In this introduction we will attempt to define nutritional ecology and its relationship to functional ecology, justify why it warrants a special issue, and summarise the scope of the issue. Nutritional ecology is the trophic branch of functional ecology. It is therefore useful in defining nutritional ecology to reflect on previous discussions that have appeared in this journal on the aims and scope of functional ecology (Calow 1987; Calow & Grace 1987; Bradshaw 1987; Grime 1987; Fryer 1988; Feder & Block 1992; Keddy 1992; Gaston & Robinson 2002; Fox et al. 2008). Accordingly, nutritional ecology is the organism-centred field of ecological research that is primarily focused on nutrition. Nutritional ecologists are interested in process rather than just property, and adaptation is an important part of their thinking. Although principally concerned with organism-level measurements (e.g. behaviour, physiology, and morphology), interest in these traits is derived from the ecological context: the ways in which they influence and are influenced by the ecological milieu. Nutritional ecology is thus a fundamentally integrative science, which seeks to explain ecological phenomena with reference to organismal mechanisms and, conversely, to understand organismal traits in relation to the ecological context in which they evolved (see also Raubenheimer et al. 2009). Given the central place of trophic interactions in ecological communities, it might be expected that the nutritional branch of functional ecology would command a high profile. Surprisingly, this is not the case. As a coarse illustration, we performed an ISI Web of Science topic search to compare across successive decades the numbers of studies at the nutrition–ecology interface with the number at the physiology–ecology, behaviour–ecology and evolution–ecology interfaces. For this, we entered into the ‘Topic’ field the search terms [ecolog* and nutri*], [ecolog* and physiol*], [ecolog* and behav*] or [ecolog* and evolution*]. Figure 1 shows that for the period before 1991, ‘nutrition’ consistently scored the lowest number of hits, and thereafter exceeded only ‘physiology’ but remained substantially lower than ‘behaviour’ and ‘evolution’. To evaluate the extent to which those studies at the nutrition–ecology interface were identified by the authors as ‘nutritional ecology’, we performed a second search comparing the number of hits retrieved for [‘nutritional ecology’], [‘behavioural ecology’or‘behavioral ecology’], [‘physiological ecology’] and [‘evolutionary ecology’]. Figure 2 shows that across all decades the term ‘nutritional ecology’ was used less frequently than ‘physiological ecology’, ‘behavioural ecology’ or ‘evolutionary ecology’. Number of hits returned from ISI Web of Science for searches using the topic terms [ecolog* and nutri*], [ecolog* and physiol*], [ecolog* and behav*] or [ecolog* and evolution*] (18 November 2008). Data are presented separately for successive decades from 1960 to present. Topics terms search the following fields: title, abstract, author keywords, keywords plus®. Number of hits returned from ISI Web of Science for searches using the topic terms [‘nutritional ecology’], [‘physiological ecology’], [‘behavioural ecology’or‘behavioral ecology’], or [‘evolutionary ecology’] (18 November 2008). Data are presented separately for successive decades from 1960 to present. Topics terms search the following fields: title, abstract, author keywords, keywords plus®. This analysis, albeit crude, emphasises three points. First, the union of ‘nutrition’ and ‘ecology’ is under-represented in the literature. We acknowledge that there are probably a large number of studies that by some criteria can be classified as ‘nutritional ecology’ but are not represented in Fig. 1: for example, studies that include as Topic words both ‘ecology’ and ‘energy’ or ‘foraging’ (but not ‘nutrition’). The search was specifically designed to exclude these, to emphasise our second point: the importance of nutrition in nutritional ecology. Arguably, studies that consider foraging, for example, but do not investigate the nutritional underpinnings, or assume that energy is the foraging currency, fall under the banner of behavioural ecology, but not nutritional ecology (Raubenheimer et al. 2009). The third point that this analysis emphasises is that the label ‘nutritional ecology’ has not penetrated as deeply into the scientific lexicon as ‘physiological ecology’, ‘behavioural ecology’ or ‘evolutionary ecology’. This is illustrated both by the low absolute number of hits on ‘nutritional ecology’ (Fig. 2), and the low proportion of studies at the nutrition–ecology interface that used this term [e.g. from 1991 to the present the number of hits for ‘physiological ecology’ was higher than ‘nutritional ecology’ (Fig. 2), even though there were more papers at the nutrition–ecology interface than the physiology–ecology interface (Fig. 1)]. Labels such as ‘nutritional ecology’ are of more than cosmetic importance. At the least they provide ‘a psychological symbol of a willingness to emphasize new directions’ (Feder & Block 1991), but they also foster a unity of purpose needed to seed the infrastructure for developing new directions – societies, conferences, books, journals and institutions. In our judgement, the importance of nutrition in ecology, the limited penetration of ‘nutritional ecology’ and the dearth of studies that can be classified as nutritional ecology sensu stricto make a compelling case for new initiatives in this area. We believe that Functional Ecology provides an ideal forum for such an initiative. We open the special feature with an analysis by Raubenheimer et al. (2009) of the requirements for a solid conceptual framework for nutritional ecology: it must be nutritionally, organismally, and ecologically explicit. They then ask: Do the available major approaches to the field satisfy these requirements? Can any be expanded to do so, and what might we learn from such an expansion? The answers demonstrate the power of nutritional ecological approaches to solve outstanding problems at diverse levels of biological organization. From this broad conceptual base for the field, we move to methodology and its associated underlying theory. One of nutritional ecology's hallmark techniques is stable isotope analysis, which has facilitated a dramatic increase in our ability to understand nutritional processes in living organisms. Wolf et al. (2009) provide a review of progress in use of stable isotopes in diverse areas of nutritional ecology over the past 10 years, highlighting areas where further empirical and theoretical understanding is needed. Three sets of papers focused on different organismal study systems follow. Each system showcases different strengths of the application of the integrative aspects of the nutritional ecology paradigm. The first study system is insects, including their symbionts. Boggs (2009) utilizes a resource acquisition and allocation framework as a template to understand linkages among foraging and life history traits in insects, including patterns of senescence, under benign and stressful environments. This framework is critical to understanding the processes underlying life history and senescence, yet much remains to be done, particularly in wild populations and diverse insect taxa. Douglas (2009) presents a complementary view, examining the role of microbial symbionts of insects in facilitating plant utilisation, and consequently the very high abundance and wide distribution of insects. She highlights the emerging role of genomic tools to examine metabolic capabilities of both insects and microorganisms, expanding the feasibility of understanding the role of nutritional ecology in shaping the broader ecological characteristics of these symbioses. The second organismal study system focuses on herbivorous terrestrial mammals. Plants are well-protected against herbivory by several means, including natural toxins. Torregrossa & Dearing (2009) compare two models that could explain how mammals avoid being poisoned by their plant food, and then discuss mechanisms underlying those models. Nutritional ecology is highlighted here in the classic sense of the factors regulating nutrient acquisition, with a strong focus on the underlying physiology. Parker et al. (2009) focus on body condition as a key determinant of the integration between nutrient acquisition and nutrient demand in ungulates living in seasonal environments, and show that this integration critically influences life history traits. With its focus on life history traits, this analysis has parallels to that of Boggs (2009) presented earlier for insects. Parker et al. (2009) noted that their analysis has management implications, extending the relevance of nutritional ecology to include wildlife management and conservation. Last in this group, Felton et al. (2009) bring behaviour to the fore, with an examination of five proposed nutritional goals used to explain diet selection by primates. These include maximization of various nutrient types or energy, minimization or limitation on intake of some diet components, and nutrient balancing. The authors argue that primate nutritional ecology could benefit from the adoption of models and observational methodologies used in other organisms. This applies not only to primates, but more broadly, and one goal of this feature is to facilitate the appropriate spread of models and methodologies within the field. Moving from endotherms to ectotherms, the feature closes with consideration of the nutritional ecology of marine herbivorous fish, comparing this field with our understanding in terrestrial systems (Clements et al. 2009). Marine herbivorous fish can function as keystone species in structuring reef systems, highlighting the importance of understanding their nutritional ecology. The authors argue that more work is needed at the core of nutritional ecology, that is, food nutritional composition and the physiology of nutrient extraction and utilization. The feature as a whole reflects the broad intellectual scope of nutritional ecology, from behaviour, physiology and morphology through evolution and ecology, along with some breadth in the kinds of taxa considered. What emerges is a picture of the ubiquity of the role of nutrition as a mechanistic influence, emphasising the importance of consolidating the field that focuses on the interface of these mechanisms with ecology.