The Journal of Applied Ecology: Fifty years of scientific impact
Edited by Jos Barlow, Marc Cadotte, Rob Freckleton, Philip E. Hulme, E.J. Milner-Gulland, Stephen. J. Ormerod, Andrew R. Watkinson & Mark J. Whittingham
To mark the 50th year of the Journal of Applied Ecology, a group of current and past Editors have selected 2–3 papers per decade for a Virtual Issue, exemplifying the contribution made by our authors in framing and responding to the key applied ecological issues of the time. These papers were selected from the ten most-cited papers from each decade. Of course citation rates are not the only, or perhaps even the best, measure of the real-world impact of articles (see our Editorial on the Journal's role in promoting the impact of applied ecology; Milner-Gulland et al. 2012). However, citations highlight those papers that have been recognized as important by the authors' peers, and by the following generations of authors, and so are a useful first cut. We also saw this highly cited set of papers as an interesting insight into the research and management priorities of different decades. In the 1960s, methodological advances in ecology were key. This methodological streak continues through the following decades, but we also see the emergence of papers that provided the fundamental information needed to create meaningful policy, and latterly to evaluate its effectiveness. The 1980s was a particularly interesting decade, marking the emergence of studies on climate change and on ecosystem services, though at that point the ecosystem services concept was not labelled as such.
This Virtual Issue is not intended to be an unbiased or comprehensive history of applied ecology. However, we hope that our selection will interest and intrigue readers, and promote reflection on how the application of ecological science has developed over the 50 years of the Journal, and how the work of ecologists has both revealed and solved environmental problems.
The first decade of the Journal of Applied Ecology found the Journal publishing a wide range of topics including the performance of crops, their pests and weeds, the impact of pollution on species and ecosystems, and the impacts of grazing animals on the environment. From the start, the Journal had a global outlook with publications drawn from ecosystems around the world. Surprisingly, given the launch of the journal less than two years after the publication of Rachel Carson’s Silent Spring (Carson 1962), studies describing the impact of pollution on wildlife only appeared towards the end of the decade, although the Journal did publish early classics in this field, such as Ratcliffe (1970). Instead, much of the focus was on improving the productivity of agricultural ecosystems rather than addressing the potential impact of agriculture on species conservation. The reputation of the Journal as a medium for the publication of methodological approaches also became increasingly evident. Although today some of these methodological insights might appear a little esoteric – such as the Journal’s most cited paper “A method of estimating total length of root in a sample” by Newman (1966) – others were more clearly tied to ecological management. Among the most-cited papers published between 1964 and 1970, two methodological papers stand out that illustrate that quantitative and modelling techniques were already important in applied ecological science. While it may not be everybody’s idea of applied ecology, examining the contents of animal faeces to estimate diet has often played a pivotal role in ecosystem management. Stewart (1967) published one of the first quantitative techniques for assessing dietary content of grazing herbivores, specifically the grass diet of wildebeest Connochaetes taurinus and zebras Equus burchellii, by examining epidermis fragments under a light microscope. The paper spurred further investigations of faecal dietary analysis using the same or similar techniques, extending to numerous herbivores ranging from rice rats Oryzomys spp. to rhinos (family Rhinocerotidae). Faecal analysis is now part of the standard toolkit for many ecologists interested in individual behaviour and aggregate food webs, and the approach adopted by Stewart (1967) remains an important reference for the study of resource partitioning among ungulates in African savannas.
An early application of matrix models to resource management was published by Usher (1966), who applied a Leslie matrix to investigate the sustainable harvest of forest timber. The paper represents one of the first applications where size was substituted for age in the matrix structure, leading to a much more flexible and generalizable model structure. The paper illustrates the importance of modelling papers going beyond the development of the model to provide examples of its application in order to improve the concrete relevance of the study to other researchers. Usher (1966) applied his model to a stand of Scots pine Pinus sylvestris and provided parameters for how much timber and which size classes might be removed to maximize subsequent forest productivity. Matrix models have, for a number of decades, been the cornerstone of approaches simulating the management of species of conservation concern as well as pests; many of these models have their roots in this seminal paper.
The papers in the Journal’s second decade reflect the need for basic information about the biology of species with large economic impacts. While many of the papers we currently publish use ecological information and concepts to evaluate or promote management strategies, in the 1970s this basic information about the species being managed was still lacking. During this period of rapid agricultural expansion and modernization, exemplified by the so-called ‘green revolution’, researchers were acutely concerned with pests that lowered crop productivity. Some of our top cited papers from this decade researched aphid population biology, such as how their population growth can be simulated using simple models (Wyatt & White 1977), which predators cause the most mortality (Edwards et al. 1979), or how they respond to different temperatures (Campbell et al. 1974). Beyond understanding insect pest dynamics, some other aspects of the basic biology of economically important species and systems appeared. These papers included an examination of how water availability affects Sitka Spruce Picea sitchensis tissue (Hellkvist et al. 1974), and how barley Hordeum vulgare growth is affected by temperature and rainfall. Further, two papers explored how forests interact with the abiotic environment, with one examining the influence of solar radiation on tropical forest productivity (Monteith 1972), whilst the other described a model predicting how a forest intercepts rainfall (Rutter et al. 1975).
In our first chosen paper, Cromartie (1975) examined how the patch characteristics of collards Brassica oleracea influenced colonization dynamics of pest insects, and specifically showed that a combination of patch size and the identity of co-occurring crop species had strong effects on arthropod composition and abundance. This paper is of particular interest because it was published in an era of widespread pesticide use and it reveals how ecological factors can drastically alter pest prevalence. Segments of modern agriculture have adopted organic, low-impact practices, and a paper like Cromartie’s provides early evidence that certain management practices can reduce the risk of pest outbreaks. The other paper we feature is methodological, and serves as an early illustration of the strong succession of methodological papers in the Journal. It describes a computer program that estimates the most appropriate model describing plant growth (Hunt & Parsons 1974). This paper is highly cited because it not only describes a useful computer program to fit growth models, but perhaps more importantly it lays out the theory behind fitting growth models nicely, showing how certain parameters should be estimated.
The timing of events in the life cycle of species has long been of interest, particularly in relation to spring, with the arrival of swallows, the first sightings of frog spawn, the flowering of spring herbs and bud burst in trees. In the early 1980s there was considerable interest in the phenology of trees in spring because of its importance in assessing the probability of spring frost damage, in modelling tree growth and in assessing the likely damage from defoliating insects (Cannell & Smith 1983). Such studies provided considerable evidence that the thermal time to bud burst (days with temperature >5°C since 1 January) decreases with increased duration of previous chilling (number of days <5°C since 1 November). The timing of bud burst was thus determined by an interaction between the extent of chilling over the winter and the warmth of late winter and early spring.
With an increasing awareness of climate warming preceding the first assessment report of the Intergovernmental Panel on Climate Change in 1990, ecologists began to exploit their understanding of phenology to explore the potential impacts of climate change on biodiversity. Building on their previous work, exemplified by Cannell & Smith's 1983 paper, Murray, Cannell & Smith (1989) concluded that the effect of climatic warming on the date of bud burst would depend critically upon which part of the thermal time-chilling curve the species were on. At the time they concluded that climate warming would have little impact on bud burst at lowland sites but that bud burst in species with small chilling requirements would occur earlier at cool upland sites. This was one of a number of pioneering studies exploring the potential impacts of climate change on plant phenology. Subsequently there has been a huge increase in the number of phenological observations in relation to climatic warming in spring (Menzel et al. 2006). These have largely confirmed that phenological responses to climate change match the warming pattern (Rosenzweig et al. 2007). It is only relatively recently, however, that we have begun to understand some of the molecular mechanisms underlying the different species’ responses to climate warming with respect to flowering, leaf unfolding and bud burst (Kumar et al. 2012).
The science around the biological effects of climate change was founded in ongoing phenological research that was ready to provide answers to new policy-relevant questions. However, sometimes in science, and some would argue often, the same ideas come around again but are re-branded with new terminology. In our third paper from the 1980s, Sunderland et al. (1987) could be considered, in modern parlance, to have been exploring the importance of individual species as providers of ecosystem services; in this case as natural crop predators in the place of pesticides. This question is still of much interest given the high (economic) cost of pesticides and their strong negative effects on biodiversity. The authors studied which predators were responsible for eating cereal aphids, a major pest of many widely grown cereals such as wheat. They found that spiders played an unexpectedly significant role in aphid predation, although beetles, the expected ‘chief pest chompers’, were still considered key. Work such as this is currently much needed by those wishing to understand the interplay between individual species (often the focus of conservation effort) and the associated ecosystem services provided by those species. The answers to these types of questions are non-trivial. As shown in a recent Science paper, even understanding the food webs on one individual farm is a major achievement (Pocock, Evans & Memmott 2012). However, pioneering fundamental work, such as that by Sunderland et al., is vital to those wishing to understand how the ecosystem services concept can (or cannot) be used as an umbrella for the conservation of wider biodiversity.
Some of the Journal’s most productive authors during the 1990s wrote on themes such as heathland restoration (Rob Marrs), shorebird ecology (John Goss-Custard), large herbivores (Iain Gordon) and other mammals (David Macdonald). Major high-impact papers also revealed key field methods, for example for determining nutrient dynamics (Koerselman & Meuleman 1996), or were analytical contributions that have since underpinned key developments in predicting organism distribution under global change (Augustin, Mugglestone & Buckland 1996). The breadth and richness of the Journal’s content from outside the UK – for example studies into tropical forest fragmentation (Turner 1996) – also began to strengthen in this decade, and subsequently our authorship developed into its current highly international proportions.
Overwhelmingly, however, a key theme of the decade stemmed from increasing evidence that the management of agricultural land could have consequences for biodiversity and nature conservation. Although it had been realised since the 1960s that agriculture could affect negatively the distribution, abundance and composition of some organisms (c.f. Carson 1962), only during the 1990s was this perception given a firm quantitative scientific basis. The papers we have selected for this decade exposed the effects of agricultural management on farmland birds, and this work has gone on to have major impact.
Siriwardena et al. (1998) for the first time gave us a firm quantitative picture of the large-scale trends in bird diversity on farmland using the unique long-term data held by the British Trust for Ornithology. These data, collected by volunteers since the early 1960s, provided a detailed picture of the changes in bird populations on farmland during a period of exceptional intensification of agriculture. The analyses revealed time points at which there had been abrupt changes in population trends. For many species the mid-1970s were a period during which there was a clear marked deterioration in population numbers.
While Wilson et al. (1997), produced ground-breaking data that unequivocally linked intensification to deterioration in the breeding success of a rapidly declining species (skylark Alauda arvensis), the debate about the roles of different factors remained controversial. It was Chamberlain et al. (2000) who linked habitat changes directly to population trends. These authors were able not only to relate changes in population numbers to intensification, but also they showed a lag in the response of bird populations to agricultural practice: the worst impacts of intensification were not seen in some cases until 5 years or more after habitats changed. The Journal of Applied Ecology went on to become one of the most instrumental and influential journals in the world in publishing the basic underpinning science that subsequently had major impacts on conservation and policy. For example, farmland birds are a now key indicator group for farmland biodiversity in the UK and Europe.
There was also an intriguing extension to this work. Although the Journal’s papers were among some of the most highly cited ever to show how negative effects on nature conservation could arise from agriculture, a more overlooked feature of the Journal’s outputs in the 1990s was some of the initial work to find solutions. Thus, in one the decade's highly cited contributions, Bignal & McCracken (1996) identified the contribution of low intensity farmland to nature conservation. In words that now seem prophetic, Bignal & McCracken advocated that “the processes that make the low-intensity farmed countryside biologically rich and diverse must be understood”. The Journal of Applied Ecology was not only about identifying problems, its authors also found solutions. From 2000 onwards, developing as a journal that not only reported the research dimensions of applied ecology, but showed the value of the subject as a problem-solving discipline, for the first time on any British Ecological Society publication a strapline appeared under the Journal title; “Communicating the Value of Ecology”. This reflected an increased emphasis on linking high-quality science to management and policy, and a tangible shift in the direction of the journal.
In the first decade of the 21st century the Journal of Applied Ecology was characterised by studies on biodiversity, reflecting the global interest in conserving biodiversity in landscapes that were increasingly dominated by human activities. Highly cited papers presented methodological and statistical improvements in the analysis of survey data, including developments in wildlife density estimates using distance sampling, species distribution modelling and occupancy analysis. These models are fundamental to applied ecology and conservation: we will never sample everywhere, yet management decisions require information about broad geographic areas. In our first selected paper, Manel, Williams & Ormerod (2001) demonstrated that the accuracy of species distribution models could be improved by accounting for species prevalence (the number of times a species is recorded). Prior to their article, most species distribution modelling was based on a simple metric of presence–absence (whether a species is recorded or not). The proliferation of articles on species distribution modelling published since Manel, Williams & Ormerod (2001), and the use of this work across very many scientific fields, demonstrates how the Journal’s work underpinned the rapid development of more accurate statistical models for informing management decisions.
The decade also featured many articles that evaluated schemes introduced to maintain or enhance biodiversity in agricultural landscapes. Many billions have been spent on attempts to improve biodiversity in agricultural landscapes – for example, the European Union (EU) alone spent over €24 billion on agri-environment schemes between 1994 and 2003 (Kleijn & Sutherland 2003). Was this money well spent? Twenty years after their inception, Kleijn & Sutherland (2003) found very little scientific evidence to assess the effectiveness of these agri-environmental schemes. Their systematic review of the evidence based on 62 studies from the EU showed that research effort was strongly biased to just two countries (the Netherlands and the UK). Moreover, most studies at that time had experimental designs unlikely to provide robust results. By suggesting some simple remedies – such as adequate replication and choosing appropriate baselines – Kleijn & Sutherland pointed the way to a more robust approach to sampling, which should lead to better decision-making by policy makers. Although they cover very different topics, the articles of Kleijn & Sutherland (2003) and Manel, Williams & Ormerod (2001) are linked in an important way; both stimulated new areas of scientific enquiry that have improved our ability to detect and predict patterns of biodiversity and contribute to more robust and effective environmental policies.
Our selection of twelve papers spanning the years from 1964 to 2010 chart the development of applied ecology as a maturing scientific discipline. The papers develop novel and fundamental methods for answering scientific questions, apply these methods to important and policy-relevant questions in conservation and natural resource management, and then in later years evaluate the effectiveness of policy in producing the desired outcomes. These remain important criteria for publication in the Journal of Applied Ecology today, where the huge volume and quality of papers now being submitted allows an even stronger emphasis on papers having a broad interest beyond a specific location or species, and being directly and explicitly relevant to management or policy. The list of papers we have chosen is far from exhaustive, and other editors may have chosen a different set of significant papers that capture the science of each decade. The breadth and depth of high-quality and highly cited studies available across time is testament to the success of the Journal of Applied Ecology.
The final paragraph of the Journal’s first Editorial states:
“In our time, as the need to expand the output of food for the rapidly rising population of the world becomes more acutely felt, and as development accelerates throughout the world, the scope and tasks of applied ecology cannot but increase. Ours is an age in which ecological thinking and methods have more than ever before to contribute to the progress of mankind: the Journal of Applied Ecology hopes to play a useful part in the common effort” (Bunting & Wynne-Edwards 1964).
These words still resonate today, as we enter our next 50 years of publishing the best applied ecological science, with the aim of supporting society to resolve environmental problems and move our planet to a more sustainable future.
(hover over hyperlink for an excerpt)
Usher, M. B (1966) A Matrix Approach to Management of Renewable Resources with Special Reference to Selection Forests. Journal of Applied Ecology, 3, 355-367
Stewart, D. R. M. (1967) Analysis of Plant Epidermis in Faeces: A Technique for Studying the Food Preferences of Grazing Herbivores. Journal of Applied Ecology, 4, 83-111.
Hunt, R., & Parsons, I. T. (1974) A Computer Program for Deriving Growth-Functions in Plant Growth-Analysis. Journal of Applied Ecology, 11, 297-307.
Cromartie, W. J. (1975) The Effect of Stand Size and Vegetational Background on the Colonization of Cruciferous Plants by Herbivorous Insects. Journal of Applied Ecology, 12, 517-533.
Cannell, M. G. R. & Smith, R. I. (1983) Thermal time, chill days and prediction of budburst in Picea sitchensis. Journal of Applied Ecology, 61, 237-249.
Sunderland, K. D., Crook, N. E., Stacey, D. L. & Fuller, B. J. (1987) A Study of Feeding by Polyphagous Predators on Cereal Aphids Using Elisa and Gut Dissection. Journal of Applied Ecology, 24, 907-933.
Murray, M. B., Cannell, M. G. R. & Smith, R. I. (1989) Date of budburst of fifteen tree species in Britain following climatic warming. Journal of Applied Ecology, 26, 693-700.
Bignal, E. M. & McCracken, D. I. (1996) Low-intensity farming systems in the conservation of the countryside. Journal of Applied Ecology, 33, 413-424.
Siriwardena, G. M., Baillie, S. R., Buckland, S. T., Fewster, R. M., Marchant, J. H. & Wilson, J. D. (1998) Trends in the abundance of farmland birds: a quantitative comparison of smoothed Common Birds Census indices. Journal of Applied Ecology, 35, 24–43.
Chamberlain, D. E., Fuller, R. J., Bunce, R. G. H., Duckworth, J. C. & Shrubb, M. (2000) Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Journal of Applied Ecology, 37, 771–788.
Manel, S., Williams, H. C. & Ormerod, S.J. (2001) Evaluating presence–absence models in ecology: the need to account for prevalence. Journal of Applied Ecology, 38, 921–931.
Kleijn, D. & Sutherland, W. J. (2003) How effective are European agri-environment schemes in conserving and promoting biodiversity? Journal of Applied Ecology, 40, 947–969.
Augustin, N. H., Mugglestone, M. A. & Buckland, S. T. (1996) An autologistic model for the spatial distribution of wildlife. Journal of Applied Ecology, 33, 339-347.
Bunting, A. H. & Wynne-Edwards, V. C. (1964) Editorial Journal of Applied Ecology, 1, 1-2.
Carson, R., Darling, L. % Darling, L. (1962) Silent spring. Boston, Houghton Mifflin, Cambridge, MA, Riverside Press.
Koerselman, W. & Meuleman, A. F. M. (1996) The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33, 1441-1450.
Kumar, S. V., Lucyshyn, D., Jaeger, K. E., Alos, E., Alvey, E., Harberd, N. P. & Wigge, P. A. (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature, 484, 242-245.
Milner-Gulland, E. J., Barlow, J., Cadotte, M. W., Hulme, P. E., Kerby, G. & Whittingham, M. J. (2012), Ensuring applied ecology has impact. Journal of Applied Ecology, 49: 1–5.
Menzel, A., Sparks, T. H., Estrella, N., Koch, E., Aasa, A., Ahas, R., Alm-Kubler, K., Bissolli, P., Braslavska, O., Briede, A., Chmielewski, F. M., Crepinsek, Z., Curnel, Y., Dahl, Å., Defila, C., Donnelly, A., Filella, Y., Jatczak, K., Mage, F., Mestre, A., Nordli, Ø., Penuelas, J., Pirinen, P., Remisova, V., Scheifinger, H., Striz, M., Susnik, A., van Vliet, A. J. H., Wielgolaski, F.-E., Zach, S. & Zust, A. (2006) European phenological response to climate change matches the warming pattern. Global Change Biology, 12: 1969–1976.
Pocock, M. J. O., Evans, D. M. & Memmott, J. (2012) The robustness and restoration of a network of ecological networks. Science, 335, 973-977.
Turner, I. M. (1996) Species loss in fragments of tropical rain forest: A review of the evidence. Journal of Applied Ecology, 33, 200-209.
Wilson, J. D., Evans, J., Browne, S. J. & King, J. R. (1997) Territory distribution and breeding success of skylarks Alauda arvensis on organic and intensive farmland in southern England. Journal of Applied Ecology 34, 1462-1478.
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