The culture of marine ecology

Marine algal ecology today faces many of the same problems as ecology in general, e.g. lack of generality of experimental results, the difficulty of making long-term predictions, and an apparent lack of agreement as to what constitutes the proper or `acceptable' way of doing this particular component of science. These problems, if real, affect marine algal ecology everywhere but, in different geographical areas, specific problems also occur; science in parts of Asia has some problems different from those in other parts of the world. Since its inception, research in marine algal ecology has been motivated by many factors, ranging from traditional needs, to curiosity, to survival, to new technology, and economic needs. Each of these has shaped the questions that have been asked by, and the level of support society has been willing to supply to, ecology. For example the requisites of tradition pushed marine ecology to ask questions about food and ceremonial biota, and our fears today about loss of biota are pushing for answers to questions about the means of preserving biodiversity. The limitations of many marine ecological studies have been pointed out by different individuals. Their comments have been valuable in forcing us to examine what we are doing as marine ecologists, and how we are doing it. Ecology, and marine algal ecology with it, has been accused of carrying out small-scale studies that have no greater generality than the sites at which the studies were done, and of using statistical procedures that are wrong or inappropriate; also, there is disagreement within the ecological community of how to correct for these `faults'. Some of the problems arise due to the nature of our particular science, e.g. working with organisms with differing genetic makeup and sensitivity of experimental results to small changes in initial conditions. Other problems are more likely due to the individuals doing the science, e.g. an inability to be an `expert' on all areas of knowledge required for a modern ecologist (taxonomy, experimental design, data analysis, etc.), and perhaps an unwillingness to recognize that in some instances different methods of data analysis are applicable and valid. As ecologists, we must come to grip with these problems, both for the sake of our science, and for our own sake as practicing ecologists.     

Intrinsically generated coloured noise in laboratory insect populations

What are the mechanisms responsible for generating the erratic fluctuations observed in natural populations? This question has been at the centre of a long debate in contemporary ecology. The irregularities in the patterns of population abundance were initially mostly attributed to environmental factors. In the mid-1970s, however, it was proposed that these fluctuations may be generated intrinsically, by the underlying nonlinearities inherent in population processes. More recently, the focus of this argument has turned increasingly towards the statistical properties of population fluctuations, with many studies showing that ecological systems tend to be dominated by low-frequency or long-term dynamics, termed ''red'' noise. Currently, the source of the ''redness'' in ecological time-series is hotly debated, with the general consensus being that environmental variables are the major driving force. Here we show that three classic laboratory populations known to display irregular fluctuations also have reddened spectra. Furthermore, the dynamics of these populations show very well-defined generic scaling properties in the form of power laws. These results imply that long-term influences in ecological systems can be the product of intrinsic dynamics.     

Assessing the impact of climate variation on survival in vertebrate populations

Abstract The impact of the ongoing rapid climate change on natural systems is a major issue for human societies. An important challenge for ecologists is to identify the climatic factors that drive temporal variation in demographic parameters, and, ultimately, the dynamics of natural populations. The analysis of long-term monitoring data at the individual scale is often the only available approach to estimate reliably demographic parameters of vertebrate populations. We review statistical procedures used in these analyses to study links between climatic factors and survival variation in vertebrate populations. We evaluated the efficiency of various statistical procedures from an analysis of survival in a population of white stork, Ciconia ciconia, a simulation study and a critical review of 78 papers published in the ecological literature. We identified six potential methodological problems: (i) the use of statistical models that are not well-suited to the analysis of long-term monitoring data collected at the individual scale; (ii) low ratios of number of statistical units to number of candidate climatic covariates; (iii) collinearity among candidate climatic covariates; (iv) the use of statistics, to assess statistical support for climatic covariates effects, that deal poorly with unexplained variation in survival; (v) spurious detection of effects due to the co-occurrence of trends in survival and the climatic covariate time series; and (vi) assessment of the magnitude of climatic effects on survival using measures that cannot be compared across case studies. The critical review of the ecological literature revealed that five of these six methodological problems were often poorly tackled. As a consequence we concluded that many of these studies generated hypotheses but only few provided solid evidence for impacts of climatic factors on survival or reliable measures of the magnitude of such impacts. We provide practical advice to solve efficiently most of the methodological problems identified. The only frequent issue that still lacks a straightforward solution was the low ratio of the number of statistical units to the number of candidate climatic covariates. In the perspective of increasing this ratio and therefore of producing more robust analyses of the links between climate and demography, we suggest leads to improve the procedures for designing field protocols and selecting a set of candidate climatic covariates. Finally, we present recent statistical methods with potential interest for assessing the impact of climatic factors on demographic parameters.     

Could ecologists be more random? Straightforward alternatives to haphazard spatial sampling

When conducting field studies, it is common for ecologists to choose the locations of sampling units arbitrarily at the time sampling occurs, rather than using a properly randomised sampling design. Unfortunately, this ‘haphazard’ sampling approach cannot provide formal statistical inference from the sample to the population without making untestable assumptions. Here, we argue that two recent technological developments remove the need for haphazard sampling in many situations. A general approach to simple randomised sampling designs is outlined, and some examples demonstrate that even complicated designs can be implemented easily using software that is widely used among ecologists. We consider that more rigorous, randomised sampling designs would strengthen the validity of the conclusions drawn from ecological studies, to the benefit of the discipline as a whole.     

Distinguishing technology from biology: a critical review of the use of GPS telemetry data in ecology

In the past decade, ecologists have witnessed vast improvements in our ability to collect animal movement data through animal-borne technology, such as through GPS or ARGOS systems. However, more data does not necessarily yield greater knowledge in understanding animal ecology and conservation. In this paper, we provide a review of the major benefits, problems and potential misuses of GPS/Argos technology to animal ecology and conservation. Benefits are obvious, and include the ability to collect fine-scale spatio-temporal location data on many previously impossible to study animals, such as ocean-going fish, migratory songbirds and long-distance migratory mammals. These benefits come with significant problems, however, imposed by frequent collar failures and high cost, which often results in weaker study design, reduced sample sizes and poorer statistical inference. In addition, we see the divorcing of biologists from a field-based understanding of animal ecology to be a growing problem. Despite these difficulties, GPS devices have provided significant benefits, particularly in the conservation and ecology of wide-ranging species. We conclude by offering suggestions for ecologists on which kinds of ecological questions would currently benefit the most from GPS/Argos technology, and where the technology has been potentially misused. Significant conceptual challenges remain, however, including the links between movement and behaviour, and movement and population dynamics.     

A truly ecological epigenetics study

Until a few years ago, epigenetics was a field of research that had nothing to do with ecology and that virtually no ecologist had ever heard of. This is now changing, as more and more ecologists learn about epigenetic processes and their potential ecological and evolutionary relevance, and a new research field of ecological epigenetics is beginning to take shape. One question that is particularly intriguing ecologists is to what extent epigenetic variation is an additional, and hitherto overlooked, source of natural variation in ecologically important traits. In this issue of Molecular Ecology, Herrera & Bazaga (2011) provide one of the first attempts to truly address this question in an ecological setting. They study variation of DNA methylation in a wild population of the rare, long-lived violet Viola cazorlensis, and they use these data to explore interrelations between environmental, genetic and epigenetic variation, and in particular the extent to which these factors are related to long-term differences in herbivore damage among plants. They find substantial epigenetic variation among plant individuals. Interestingly, this epigenetic variation is significantly correlated with long-term differences in herbivory, but only weakly with herbivory-related DNA sequence variation, which suggests that besides habitat, substrate and genetic variation, epigenetic variation may be an additional, and at least partly independent, factor influencing plant–herbivore interactions in the field. Although the study by Herrera & Bazaga (2011) raises at least as many new questions as it answers, it is a pioneering example of how epigenetics can be incorporated into ecological field studies, and it illustrates the value and potential novel insights to be gained from such efforts.     

The irreducible uncertainty of the demography-environment interaction in ecology

The interpretation of ecological data has been greatly improved by bridging the gap between ecological and statistical models. The major challenge is to separate competing hypotheses concerning demography, or other ecological relationships, and environmental variability (noise). In this paper we demonstrate that this may be an arduous, if not impossible, task. It is the lack of adequate ecological theory, rather than statistical sophistication, which leads to this problem. A reconstruction of underlying ecological processes can only be done if we are certain of either the demographic or the noise model, which is something that can only be achieved by an improved theory of stochastic ecological processes. Ignoring the fact that this is a real problem may mislead ecologists and result in erroneous conclusions about the relative importance of endogenous and exogenous factors in natural ecosystems. The lack of correct model identification may also have far-reaching consequences for population management and conservation.     

Microarray challenges in ecology

Microarrays are used to measure simultaneously the amount of mRNAs transcribed from many genes. They were originally designed for gene expression profiling in relatively simple biological systems, such as cell lines and model systems under constant laboratory conditions. This poses a challenge to ecologists who increasingly want to use microarrays to unravel the genetic mechanisms underlying complex interactions among organisms and between organisms and their environment. Here, we discuss typical experimental and statistical problems that arise when analyzing genome-wide expression profiles in an ecological context. We show that experimental design and environmental confounders greatly influence the identification of candidate genes in ecological microarray studies, and that following several simple recommendations could facilitate the analysis of microarray data in ecological settings.     

Inference in ecology and evolution

Most ecologists and evolutionary biologists continue to rely heavily on null hypothesis significance testing, rather than on recently advocated alternatives, for inference. Here, we briefly review null hypothesis significance testing and its major alternatives. We identify major objectives of statistical analysis and suggest which analytical approaches are appropriate for each. Any well designed study can improve our understanding of biological systems, regardless of the inferential approach used. Nevertheless, an awareness of available techniques and their pitfalls could guide better approaches to data collection and broaden the range of questions that can be addressed. Although we should reduce our reliance on significance testing, it retains an important role in statistical education and is likely to remain fundamental to the falsification of scientific hypotheses.     

Ecology after 100 years: Progress and pseudo-progress

Has the science of ecology fulfilled the promises made by the originators of ecological science at the start of the last century? What should ecology achieve? Have good policies for environmental management flowed out of ecological science? These important questions are rarely discussed by ecologists working on detailed studies of individual systems. Until we decide what we wish to achieve as ecologists we cannot define progress toward those goals. Ecologists desire to achieve an understanding of how the natural world operates, how humans have modified the natural world, and how to alleviate problems arising from human actions. Ecologists have made impressive gains over the past century in achieving these goals, but this progress has been uneven. Some sub-disciplines of ecology are well developed empirically and theoretically, while others languish for reasons that are not always clear. Fundamental problems can be lost to view as ecologists fiddle with unimportant pseudo-problems. Bandwagons develop and disappear with limited success in addressing problems. The public demands progress from all the sciences, and as time moves along and problems get worse, more rapid progress is demanded. The result for ecology has too often been poor, short-term science and poor management decisions. But since the science is rarely repeated and the management results may be a generation or two down the line, it is difficult for the public or for scientists to decide how good or bad the scientific advice has been. In ecology over the past 100 years we have made solid achievements in behavioural ecology, population dynamics, and ecological methods, we have made some progress in understanding community and ecosystem dynamics, but we have made less useful progress in developing theoretical ecology, landscape ecology, and natural resource management. The key to increasing progress is to adopt a systems approach with explicit hypotheses, theoretical models, and field experiments on a scale defined by the problem. With continuous feedback between problems, possible solutions, relevant theory and experimental data we can achieve our scientific goals.     

Developing an ecological context for allelopathy

There has been a renewed interest in allelopathy as a plant–plant interaction as more plant ecologists have become involved in studying biological invasions. This resurgence highlights a major deficiency in our understanding of allelopathy—the lack of a well-developed ecological context for the interaction. In contrast to allelopathy, the plant–plant interaction of competition has a strong theoretical foundation as well as a large body of supporting empirical studies. We suggest that the plant-herbivore defense literature provides a mature and well-developed framework from which a broader ecological context for allelopathy can be developed. Here, we discuss three broad classes of questions, drawn from the herbivore defense literature, which may help to develop an appropriate ecological context for allelopathy. These questions focus on (1) variation in allelopathic expression within species, (2) community level variation in allelopathy across species, and (3) variation in the impacts of allelopathy on associated species. Addressing such broad population and community level themes in a variety of systems will be necessary to fully develop an ecological context for allelopathy and provide a theoretical basis for understanding its role in plant communities.     

Developing an ecological context for allelopathy

There has been a renewed interest in allelopathy as a plant?Cplant interaction as more plant ecologists have become involved in studying biological invasions. This resurgence highlights a major deficiency in our understanding of allelopathy??the lack of a well-developed ecological context for the interaction. In contrast to allelopathy, the plant?Cplant interaction of competition has a strong theoretical foundation as well as a large body of supporting empirical studies. We suggest that the plant-herbivore defense literature provides a mature and well-developed framework from which a broader ecological context for allelopathy can be developed. Here, we discuss three broad classes of questions, drawn from the herbivore defense literature, which may help to develop an appropriate ecological context for allelopathy. These questions focus on (1) variation in allelopathic expression within species, (2) community level variation in allelopathy across species, and (3) variation in the impacts of allelopathy on associated species. Addressing such broad population and community level themes in a variety of systems will be necessary to fully develop an ecological context for allelopathy and provide a theoretical basis for understanding its role in plant communities.     

Applications of selective neutrality tests to molecular ecology

This paper reviews how statistical tests of neutrality have been used to address questions in molecular ecology are reviewed. The work consists of four major parts: a brief review of the current status of the neutral theory; a review of several particularly interesting examples of how statistical tests of neutrality have led to insight into ecological problems; a brief discussion of the pitfalls of assuming a strictly neutral model if it is false; and a discussion of some of the opportunities and problems that molecular ecologists face when using neutrality tests to study natural selection.     

Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links

A major empirical approach in community ecology is to describe the dynamics of a community by examining small subsets of species. Unfortunately, interaction modifications, which cause pair-wise interaction coefficients to depend on the presence or absence of additional species, can make it difficult to predict the overall dynamics of species within a community from experiments with pairs of species. In a similar fashion, one of the major approaches in evolutionary ecology has been to describe the likely evolutionary dynamics of a single species by focusing on the selection imposed by a limited number of other species within the community. However, recent work on diffuse coevolution indicates that selection pressures due to one species can change in the presence of other species. The magnitude of the difficulty that interaction modifications and diffuse coevolution present for predicting ecological and evolutionary dynamics is an unresolved question. Here we outline the similarities and differences between the two topics, discuss experimental and statistical approaches to studying them, and make predictions about when ecological interaction modifications are likely to cause diffuse coevolution. Since the currencies for interaction modifications are usually fitness components such as growth, fecundity, or survival, is it likely that these will translate into corresponding differences in the relative fitness of individuals or genotypes, and thus in general these two phenomena will occur together. We argue that community ecologists and evolutionary ecologists will both benefit from experiments that test for the effects of interaction modifications, and that studies of the mechanisms driving interaction modifications and diffuse coevolution (e.g., changes in behavior, nonlinear effects on shared resources, genetic covariances) will aid our progress in understanding the ecological and evolutionary dynamics of communities.     

Masting,mixtures and modes: are two models better than one?

A key hypothesis in population ecology is that synchronous and intermittent seed production, known as mast seeding, is driven by the alternating allocation of carbohydrates and mineral nutrients between growth and reproduction in different years, i.e. ‘resource switching’. Such behaviour may ultimately generate bimodal distributions of long‐term flower and seed production, and evidence of these patterns has been taken to support the resource switching hypothesis. Here, we show how a widely‐used statistical test of bimodality applied by many studies in different ecological contexts may fail to reject the null hypothesis that focal probability distributions are unimodal. Using data from five tussock grass species in South Island, New Zealand, we find clear evidence of bimodality only when flowering patterns are analyzed with probabilistic mixture models. Mixture models provide a theory oriented framework for testing hypotheses of mast seeding patterns, enabling the different responses underlying medium‐ and high‐ versus non‐ and low‐flowering years to be modelled more realistically by associating these with distinct probability distributions. Coupling theoretical expectations with more rigorous statistical approaches will empower ecologists to reject null hypotheses more often.     

Process and measurement errors of population size: their mutual effects on precision and bias of estimates for demographic parameters

Knowing the parameters of population growth and regulation is fundamental for answering many ecological questions and the successful implementation of conservation strategies. Moreover, detecting a population trend is often a legal obligation. Yet, inherent process and measurement errors aggravate the ability to estimate these parameters from population time-series. We use numerical simulations to explore how the lengths of the time-series, process and measurement error influence estimates of demographic parameters. We first generate time-series of population sizes with given demographic parameters for density-dependent stochastic population growth, but assume that these population sizes are estimated with measurement errors. We then fit parameters for population growth, habitat capacity, total error and long-term trends to the ‘measured’ time-series data using non-linear regression. The length of the time-series and measurement error introduce a substantial bias in the estimates for population growth rate and to a lesser degree on estimates for habitat capacity, while process error has little effect on parameter bias. The total error term of the statistical model is dominated by process error as long as the latter is larger than the measurement error. A decline in population size is difficult to document as soon as either error becomes moderate, trends are not very pronounced, and time-series are short (<10–15 seasons). Detecting an annual decline of 1% within 6-year reporting periods, as required for the European Union for the species of Community Interest, appears unachievable.     

How do plant ecologists use matrix population models?

Matrix projection models are among the most widely used tools in plant ecology. However, the way in which plant ecologists use and interpret these models differs from the way in which they are presented in the broader academic literature. In contrast to calls from earlier reviews, most studies of plant populations are based on < 5 matrices and present simple metrics such as deterministic population growth rates. However, plant ecologists also cautioned against literal interpretation of model predictions. Although academic studies have emphasized testing quantitative model predictions, such forecasts are not the way in which plant ecologists find matrix models to be most useful. Improving forecasting ability would necessitate increased model complexity and longer studies. Therefore, in addition to longer term studies with better links to environmental drivers, priorities for research include critically evaluating relative/comparative uses of matrix models and asking how we can use many short-term studies to understand long-term population dynamics.     

Amphibian declines: future directions

Abstract. The amphibian decline problem is complex, and there is no easy solution. I highlight four major areas of future research that should increase our ability to detect declines, elucidate their underlying mechanisms, and advance our capacity to manage and conserve amphibian populations. First, a statistically sensitive monitoring approach is necessary to determine the distribution and abundance of amphibian populations, to assess whether they are declining, and to quantify the extent of declines. Most amphibian populations characteristically fluctuate, detection probabilities may be low for many species and populations tend to decline in numbers between years more often than they increase. These traits make establishing monitoring programmes difficult and distinguishing declines from natural fluctuations challenging. It is thus necessary to determine the best monitoring techniques based on their statistical power and to use appropriate statistical methods for detecting population trends. Secondly, although amphibian population studies occur most commonly at single or few breeding sites, research should occur often at the landscape level, and conservation efforts should focus on suitable habitat (whether or not it is occupied) and dispersal capabilities of species. Metapopulation dynamics are probably important for many species, but we must be cautious how we define metapopulations. That is, the term ‘metapopulation’ is currently used to define a wide range of demographic situations in amphibian populations, each with different management implications. Thirdly, recent advances in molecular genetic techniques make it possible to infer demographic events such as effects of recent fragmentation, bottlenecks or hybridization. Molecular techniques can be used in conjunction with census surveys to bolster knowledge about demographic processes such as declines. Alternatively, in the absence of long‐term census data, molecular data can be used to infer population trends. New genomic approaches may make estimating adaptive genetic variation more feasible. Fourthly, multi‐factorial studies are needed to disentangle the complexity of the several putative causes that probably interact to cause amphibian declines. Recent studies demonstrate the value of a multi‐factorial approach, and more work is needed to elucidate the synergistic effects of multiple environmental factors affecting amphibian populations simultaneously worldwide.