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External influences on ecological theory: Report on organized oral Session 80 at the 100th Anniversary Meeting of the Ecological Society of America

The 100‐year history of the Ecological Society of America spans most of the major advances in the field of ecology, from the “niche” of Grinnell and others, to Lotka and Volterra's models of predation and competition based on the logistic growth equation, to the concept of competitive exclusion developed from experimental ecology, to genetics and evolutionary ecology and all the ramifications and specializations of these topics over the rest of the 20th and into the 21st century. The objective of this session, sponsored by the Historical Records Committee of the ESA, was to explore how ecological concepts have been shaped and changed by influences that are external to the scientific method, such as funding priorities, ideology, politics, personalities, and differences between the ecosystems where influential ecologists developed their ideas. Among the many memorable quotations of the philosopher/poet George Santayana (1863–1952) is the often quoted and misquoted observation, “Those who cannot remember the past are condemned to repeat it.”

Bulletin of the Ecological Society of America

Ecological and evolutionary consequences of benthic community stasis in the very deep sea (>1500 m)

An enigma of deep-sea biodiversity research is that the abyss with its low productivity and densities appears to have a biodiversity similar to that of shallower depths. This conceptualization of similarity is based mainly on per-sample estimates (point diversity, within-habitat, or α-diversity). Here, we use a measure of between-sample within-community diversity (β 1H ) to examine benthic foraminiferal diversity between 333 stations within 49 communties from New Zealand, the South Atlantic, the Gulf of Mexico, the Norwegian Sea, and the Arctic. The communities are grouped into two depth categories: 200–1500 m and >1500 m. β 1H diversity exhibits no evidence of regional differences. Instead, higher values at shallower depths are observed worldwide. At depths of >1500 m the average β 1H is zero, indicating stasis or no biodiversity gradient. The difference in β 1H -diversity explains why, despite species richness often being greater per sample at deeper depths, the total number of species is greater at shallower depths. The greater number of communities and higher rate of evolution resulting in shorter species durations at shallower depths is also consistent with higher β 1H values.

Arctic Ocean;Gulf Of Mexico;Norwegian Sea;South At

Adaptive breeding habitat selection: Is it for the birds?

The question of why animals choose particular habitats has important implications for understanding behavioral evolution and distribution of organisms in the wild and for delineating between habitats of different quality for conservation and management. Habitats chosen by animals can influence fitness outcomes via the costs (e.g., predation risk) and benefits (e.g., food availability) of habitat use. Habitat preferences should therefore be under selection to favor those that confer fitness advantages (Clark and Shutler 1999). Indeed, prevailing theory suggests that the habitat preferences of animals should be adaptive, such that fitness is higher in preferred habitats (Hildén 1965, Southwood 1977, Martin 1998). However, studies have often identified apparent mismatches between observed habitat preferences and fitness outcomes across a wide variety of taxa (Valladares and Lawton 1991, Mayhew 1997, Kolbe and Janzen 2002, Arlt and Pärt 2007, Mägi et al. 2009). Certainly, one limitation of studies may be that assessment of “fitness” is typically constrained to fitness surrogates such as nest success rather than lifetime reproductive success or classic Fisherian fitness (Endler 1986). Nevertheless, important habitat choices such as nest sites influence the probability that temporarily sedentary, dependent young are discovered by enemies such as predators and parasites. We therefore expect, on average, to see congruence between evolved habitat preferences and relevant components of fitness (e.g., nest success). Here, we (1) review the prevalence of apparent mismatches between avian breeding-habitat preferences and fitness outcomes using nest-site selection as a focus; (2) describe several potential mechanisms for such mismatches, including anthropogenic, methodological, and ecological–evolutionary; and (3) suggest a framework for understanding the contexts in which habitat preferences represent adaptive decisions, with a primary focus on ecological information theory. We largely focus on habitat selection as a behavioral process at the scale of individuals (e.g., Robertson and Hutto 2006), rather than at the scale of population-level patterns (Fretwell and Lucas 1970, Morris 2003, Johnson 2007). However, these two scales cannot be wholly divorced from one another, as we will discuss.

The Auk

Modeling individual animal histories with multistate capture–recapture models

Many fields of science begin with a phase of exploration and description, followed by investigations of the processes that account for observed patterns. The science of ecology is no exception, and recent decades have seen a focus on understanding key processes underlying the dynamics of ecological systems. In population ecology, emphasis has shifted from the state variable of population size to the demographic processes responsible for changes in this state variable: birth, death, immigration, and emigration. In evolutionary ecology, some of these same demographic processes, rates of birth and death, are also the determinants of fitness. In animal population ecology, the estimation of state variables and their associated vital rates is especially problematic because of the difficulties in sampling such populations and detecting individual animals. Indeed, early capture–recapture models were developed for the purpose of estimating population size, given the reality that all animals are not caught or detected at any sampling occasion. More recently, capture–recapture models for open populations were developed to draw inferences about survival in the face of these same sampling problems. The focus of this paper is on multi‐state mark–recapture models (MSMR), which first appeared in the 1970s but have undergone substantial development in the last 15 years. These models were developed to deal explicitly with biological variation, in that animals in different “states” (classes defined by location, physiology, behavior, reproductive status, etc.) may have different probabilities of survival and detection. Animal transitions between states are also stochastic and themselves of interest. These general models have proven to be extremely useful and provide a way of thinking about a remarkably wide range of important ecological processes. These methods are now at a stage of refinement and sophistication where they can readily be used by biologists to tackle a wide range of important issues in ecology. In this paper, we draw together information on the state of the art in multistate mark–recapture methods, explaining the models and illustrating their use. We provide a modeling philosophy and a series of general principles on how to conduct analyses. We cover key issues and features, and we anticipate the ways in which we expect the models to develop in the years ahead.

Advances in Ecological Research

North American Bird Banding and quantitative population ecology

Early bird-banding programs in North America were developed to provide descriptions of bird migration and movement patterns. This initial interest in description quickly evolved into more quantitative interests in two ways. There was (1) interest in quantifying migration and movement patterns, and (2) rapid recognition that re-observations of marked birds provided information about other parameters relevant to population dynamics. These included survival rate, recruitment rate, and population size. The evolution of methods for estimating population size, survival, recruitment, and movement is reviewed and we show it to be closely tied to bird-banding data. These estimation methods have been used with bird-banding data to draw important inferences about evolutionary ecology, population ecology, and population management. Illustrative examples of such inferences are provided.

Book chapter

A common garden super-experiment: An impossible dream to inspire possible synthesis

Global change threatens plant diversity and disrupts its interrelationship with ecosystem structure and function. This disruption in turn undermines confidence in the knowledge ecologists produce, and whether it will translate into multidisciplinary research settings or guide the effective management of natural lands. To address this challenge, ecology needs to consider the interactions between different levels of biological hierarchy, especially how they feedback on, and are mediated by, plant diversity. Doing so will require conducting empirical work and developing theory that simultaneously considers multiple disciplinary perspectives and units of study. Here we advocate the use of common gardens to integrate ecology, evolutionary biology, and ecosystem science through an explicit focus on simultaneous measurement of response variables at multiple levels of biological organization. This approach will provide opportunities to evaluate assumptions important to prediction, such as space-for-time substitution, and tackle the integration of physicochemical and eco-evolutionary foundations to understanding plants and ecosystems. Synthesis: We summarize the large body of research on Sonoran Desert winter annuals to demonstrate how experimental designs that employ common gardens to integrate processes across scales hold special promise. This includes refining trait-based theories of plant strategies, providing insight into ecosystem responses to global change, and collaborating effectively with other scientific disciplines.

Journal of Ecology

Deconstructing cardiovascular and coagulation-related traits links dietary ecology to multi-functional snake venom specificity

Animal venoms vary greatly in compositional complexity, where complex venoms are hypothesized to be maintained by greater dietary breadth. Beyond explaining venom composition, the dietary breadth hypothesis predicts that these more complex venoms should show greater functional breadth in terms of overall toxicity and by disrupting multiple prey physiological processes. We evaluate these predictions with six distinct physiological assays of cardiac and blood clotting functions and compared the effects of venoms from snake species with a range of taxonomic dietary diversity levels. We compared the taxonomic dietary generalists Agkistrodon piscivorus and Sistrurus miliarius to taxa with varying taxonomic specialization, namely Ag. contortrix and Crotalus adamanteus , and Azemiops feae . Comparing fish thrombocyte and mammal platelet aggregation and fibrin clot formation, only species with broader diets disrupted both fish and mammal hemostatic function. Venom of Ag. piscivorus , a uniquely fish-eating species, was the most disruptive of zebrafish heart rate, thrombocyte activation, vascular permeability, and clotting after injury. Sistrurus miliarius was also highly toxic, whereas mammal-specialists’ venoms scarcely altered zebrafish physiology. Our results support the hypothesis that dietary breadth selects functionally complex venoms. Understanding venom gene evolution, snakebite symptoms, and searching for therapeutics in venom should be guided by evolutionary ecology.

Evolution

When parasites become prey: ecological and epidemiological significance of eating parasites

Recent efforts to include parasites in food webs have drawn attention to a previously ignored facet of foraging ecology: parasites commonly function as prey within ecosystems. Because of the high productivity of parasites, their unique nutritional composition and their pathogenicity in hosts, their consumption affects both food-web topology and disease risk in humans and wildlife. Here, we evaluate the ecological, evolutionary and epidemiological significance of feeding on parasites, including concomitant predation, grooming, predation on free-living stages and intraguild predation. Combining empirical data and theoretical models, we show that consumption of parasites is neither rare nor accidental, and that it can sharply affect parasite transmission and food web properties. Broader consideration of predation on parasites will enhance our understanding of disease control, food web structure and energy transfer, and the evolution of complex life cycles.

Trends in Ecology and Evolution

Fitness homeostasis across an experimental water gradient predicts species' geographic range and climatic breadth

Species range sizes and realized niche breadths vary tremendously. Understanding the source of this variation has been a long-term aim in evolutionary ecology and is a major tool in efforts to ameliorate the impacts of changing climates on species distributions. Species ranges that span a large climatic envelope can be achieved by a collection of specialized genotypes locally adapted to a small range of conditions, by genotypes with stable fitness across variable environments, or a combination of these factors. We asked whether fitness expressed along a key niche axis, water availability, could explain a species' realized niche breadth, its geographic range and climate breadth, in 11 species from a clade of jewelflowers whose range sizes vary by two orders of magnitude. Specifically, we explored whether the range size of a species was related to the ability of genotypes (maternal families) to maintain fitness across a range of experimental water availabilities based on 30-year historical field precipitation regimes. We operationally characterized fitness homeostasis through the coefficient of variation in fitness of a genotype (family) across the experimental water gradient. We found that species with genotypes that had high fitness homeostasis, low variation in fitness over our treatments, had larger climatic niche breadth and geographic range in their field distributions. The result was robust to alternate measures of fitness homeostasis. Our results show that the fitness homeostasis of genotypes can be a major factor contributing to niche breadth and range size in this clade. Fitness homeostasis can buffer species from loss of genetic diversity and under changing climates, provides time for adaptation to future conditions.

Ecology

[Book review] Cowbirds and Other Brood Parasites by Catherine Ortega. Tucson, Arizona: University of Arizona Press (1998). The Avian Brood Parasites: Deception at the Nest by Paul A. Johnsgard. New York: Oxford University Press (1997) Parasitic Birds and their Hosts: Studies in Coevolution edited by S.I. Rothstein & S.K. Robinson. New York: Oxford University Press (1998)

We are in a golden age for the study of brood parasitism, judging from both the quantity and quality of recent scientific publications on cuckoos, cowbirds and parasitic finches by investigators working in Europe, the Americas, Africa and Asia. As Johnsgard (1997) remarks in his preface, the evolutionary, ecological, and behavioural questions posed by obligate brood parasites are among the most intriguing contemporary ornithological topics. Rothstein & Robinson (1998) explain that brood parasites make ideal subjects for testing the generality of models for the evolution of social and mating behaviour, foraging behaviour, spatial distribution, and vocal development, because the strategy of providing no parental care removes constraints imposed on other birds. Since Aristotle, people have been fascinated by brood parasites, but only in the past two decades has the number of investigators working on this topic reached a critical mass and created momentum that promises many breakthroughs. New studies are being completed so rapidly that a general book is inevitably out of date on some topics by the time it is published. A complete library on brood parasitism should add two recent volumes (Morrison et al. 1999; Smith et al., in press).to the three reviewed here.

Animal Behaviour

The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters

The quantification of individuality is a common research theme in the fields of population, community, and evolutionary ecology. The potential for individuality to arise is likely context-dependent, and the influence of habitat characteristics on its prevalence has received less attention than intraspecific competition. We examined individual diet specialization in 16 sea otter (Enhydra lutris) populations from southern California to the Aleutian Islands in Alaska. Because population histories, relative densities, and habitat characteristics vary widely among sites, we could examine the effects of intraspecific competition and habitat on the prevalence of individual diet specialization. Using observed diet data, we classified half of our sites as rocky substrate habitats and the other half containing a mixture of rocky and unconsolidated (soft) sediment substrates. We used stable isotope data to quantify population- and individual-level diet variation. Among rocky substrate sites, the slope [±standard error (SE)] of the positive significant relationship between the within-individual component (WIC) and total isotopic niche width (TINW) was shallow (0.23 ± 0.07) and negatively correlated with sea otter density. In contrast, the slope of the positive WIC/TINW relationship for populations inhabiting mixed substrate habitats was much higher (0.53 ± 0.14), suggesting a low degree of individuality, irrespective of intraspecific competition. Our results show that the potential for individuality to occur as a result of increasing intraspecific competition is context-dependent and that habitat characteristics, which ultimately influence prey diversity, relative abundance, and the range of skillsets required for efficient prey procurement, are important in determining when and where individual diet specialization occurs in nature.

Oecologia

Biogeography of freshwater mussels (Bivalvia: Unionida) in Texas and implications on conservation biology

Aim Biogeography seeks to identify and explain the spatial distributions of species and has become an important tool used by conservationists to protect and manage aquatic organisms. Texas, located in the southwestern United States, is home to 52 species of freshwater mussels, 9 of which are endemic to Texas and 7 that are endemic to Texas and neighboring states or countries. There have been two major attempts to classify this fauna into biogeographical provinces; however, both efforts relied on limited distribution information and outdated taxonomy. To address both issues, we set out to delineate biogeographic provinces for freshwater mussels in Texas by using a comprehensive distributional dataset of >28,000 records and molecular information. Location Southwestern United States. Methods We compiled community and molecular data for 48 of the 52 freshwater mussel species that occur in Texas. We performed algorithmic hierarchal cluster analysis (HCA) and nonmetric multidimensional scaling (NMDS) based on Euclidean distance to identify biogeographic groupings. We conducted a similar analysis using molecular sequence data for our target species. Results Based on the results from community and molecular data, we identified seven biogeographic provinces for freshwater mussels in Texas: Great Plains, Mississippi Embayment, Sabine-Neches, Trinity-San Jacinto, Central Texas, Rio Grande and Coastal. However, the Coastal and Great Plains provinces were not included in our analysis and were recognized based on previous work. Main conclusions Our approach integrating community and molecular datasets provides a comprehensive assessment of the biogeography of freshwater mussels in Texas, which serves as a model for future biogeographic studies. Our findings also shed light on the ecological, evolutionary and geologic processes shaping freshwater mussel communities in Texas, which is important for the conservation of remaining biodiversity in the state.

Texas

Local biotic adaptation of trees and shrubs to plant neighbors

Natural selection as a result of plant–plant interactions can lead to local biotic adaptation. This may occur where species frequently interact and compete intensely for resources limiting growth, survival, and reproduction. Selection is demonstrated by comparing a genotype interacting with con- or hetero-specific sympatric neighbor genotypes with a shared site-level history (derived from the same source location), to the same genotype interacting with foreign neighbor genotypes (from different sources). Better genotype performance in sympatric than allopatric neighborhoods provides evidence of local biotic adaptation. This pattern might be explained by selection to avoid competition by shifting resource niches (differentiation) or by interactions benefitting one or more members (facilitation). We tested for local biotic adaptation among two riparian trees, Populus fremontii and Salix gooddingii , and the shrub Salix exigua by transplanting replicated genotypes from multiple source locations to a 17 000 tree common garden with sympatric and allopatric treatments along the Colorado River in California. Three major patterns were observed: 1) across species, 62 of 88 genotypes grew faster with sympatric neighbors than allopatric neighbors; 2) these growth rates, on an individual tree basis, were 44, 15 and 33% higher in sympatric than allopatric treatments for P. fremontii, S. exigua and S. gooddingii , respectively, and; 3) survivorship was higher in sympatric treatments for P. fremontii and S. exigua . These results support the view that fitness of foundation species supporting diverse communities and dominating ecosystem processes is determined by adaptive interactions among multiple plant species with the outcome that performance depends on the genetic identity of plant neighbors. The occurrence of evolution in a plant-community context for trees and shrubs builds on ecological evolutionary research that has demonstrated co-evolution among herbaceous taxa, and evolution of native species during exotic plants invasion, and taken together, refutes the concept that plant communities are always random associations.

Arizona

Species and population specific gene expression in blood transcriptomes of marine turtles

Background Transcriptomic data has demonstrated utility to advance the study of physiological diversity and organisms’ responses to environmental stressors. However, a lack of genomic resources and challenges associated with collecting high-quality RNA can limit its application for many wild populations. Minimally invasive blood sampling combined with de novo transcriptomic approaches has great potential to alleviate these barriers. Here, we advance these goals for marine turtles by generating high quality de novo blood transcriptome assemblies to characterize functional diversity and compare global transcriptional profiles between tissues, species, and foraging aggregations. Results We generated high quality blood transcriptome assemblies for hawksbill ( Eretmochelys imbricata ) , loggerhead ( Caretta caretta ), green ( Chelonia mydas ), and leatherback ( Dermochelys coriacea ) turtles. The functional diversity in assembled blood transcriptomes was comparable to those from more traditionally sampled tissues. A total of 31.3% of orthogroups identified were present in all four species, representing a core set of conserved genes expressed in blood and shared across marine turtle species. We observed strong species-specific expression of these genes, as well as distinct transcriptomic profiles between green turtle foraging aggregations that inhabit areas of greater or lesser anthropogenic disturbance. Conclusions Obtaining global gene expression data through non-lethal, minimally invasive sampling can greatly expand the applications of RNA-sequencing in protected long-lived species such as marine turtles. The distinct differences in gene expression signatures between species and foraging aggregations provide insight into the functional genomics underlying the diversity in this ancient vertebrate lineage. The transcriptomic resources generated here can be used in further studies examining the evolutionary ecology and anthropogenic impacts on marine turtles.

BMC Genomics

Comparative demography of new world populations of thrushes (Turdus spp.): Comment

Survival and fecundity are fundamental to the study of evolutionary ecology, as they are two of the key variables influencing the constrained optimization process we call natural selection. Likewise, population managers require accurate estimates of these parameters; along with dispersal, they govern population dynamics ( Lack 1954 ) and thus are essential for predicting population change and the effects of management actions. It can be frustrating, then, when survival is difficult to estimate for certain populations, as in some avian species that exhibit a substantial degree of dispersal.

Ecology

Demographic estimation methods for plants with dormancy

Demographic studies in plants appear simple because unlike animals, plants do not run away. Plant individuals can be marked with, e.g., plastic tags, but often the coordinates of an individual may be sufficient to identify it. Vascular plants in temperate latitudes have a pronounced seasonal life–cycle, so most plant demographers survey their study plots once a year often during or shortly after flowering. Life–states are pervasive in plants, hence the results of a demographic study for an individual can be summarized in a familiar encounter history, such as 0VFVVF000. A zero means that an individual was not seen in a year and a letter denotes its state for years when it was seen aboveground. V and F here stand for vegetative and flowering states, respectively. Probabilities of survival and state transitions can then be obtained by mere counting. Problems arise when there is an unobservable dormant state, i.e., when plants may stay belowground for one or more growing seasons. Encounter histories such as 0VF00F000 may then occur where the meaning of zeroes becomes ambiguous. A zero can either mean a dead or a dormant plant. Various ad hoc methods in wide use among plant ecologists have made strong assumptions about when a zero should be equated to a dormant individual. These methods have never been compared among each other. In our talk and in Kéry et al. (submitted), we show that these ad hoc estimators provide spurious estimates of survival and should not be used. In contrast, if detection probabilities for aboveground plants are known or can be estimated, capturerecapture (CR) models can be used to estimate probabilities of survival and state–transitions and the fraction of the population that is dormant. We have used this approach in two studies of terrestrial orchids, Cleistes bifaria (Kéry et al., submitted) and Cypripedium reginae (Kéry & Gregg, submitted) in West Virginia, U.S.A. For Cleistes, our data comprised one population with a total of 620 marked ramets over 10 years, and for Cypripedium , two populations with 98 and 258 marked ramets over 11 years. We chose the ramet (= single stem or shoot) as the demographic unit of our study since there was no way distinguishing among genets (genet = genetical individual, i.e., the “individual” that animal ecologists are mostly concerned with). This will introduce some non–independence into the data, which can nevertheless be dealt with easily by correcting variances for overdispersion. Using ramets instead of genets has the further advantage that individuals can be assigned to a state such as flowering or vegetative in an unambiguous manner. This is not possible when genets are the demographic units. In all three populations, auxiliary data was available to show that detection probability of aboveground plants was m 0.995 We fitted multistate models in program MARK by specifying three states (D, V, F), even though the dormant state D does not occur in the encounter histories. Detection probability is fixed at 1 for the vegetative (V) and the flowering state (F) and at zero for the dormant state (D). Rates of survival and of state transitions as well as slopes of covariate relationships can be estimated and LRT or the AIC machinery be used to select among models. To estimate the fraction of the population in the unobservable dormant state, the encounter histories are collapsed to 0 (plant not observed aboveground) and 1 (plant observed aboveground). The Cormack–Jolly–Seber model without constraints on detection probability is used to estimate detection probability, the complement of which is the estimated fraction of the population in the dormant state. Parameter identifiability is an important issue in multi state models. We used the Catchpole–Morgan–Freeman approach to determine which parameters are estimable in principle in our multi state models. Most of 15 tested models were indeed estimable with the notable exception of the most general model, which has fully interactive state- and time-dependent survival and state transition rates. This model would become identifiable if at least some plants would be excavated in years when they do not show up aboveground. Our analyses for three analyzed populations of Cleistes and Cypripedium yielded annual ramet survival rates ranging from 0.86–0.96. Estimates of the average fraction dormant ranged from 0.02–0.30, but with up to half a population in the dormant state in some years. Ultrastructural modeling enables interesting hypotheses to be tested about the relationships of demographic rates with climatic covariates for instance. Such covariate modeling makes the CR approach particularly interesting for evolutionary–ecological questions about, e.g., the adaptive significance of the dormant state.

Animal Biodiversity and Conservation