Beyond Kuhnian paradigms: Normal science and theory dependence in ecology.

The Structure of Scientific Revolutions by Thomas Kuhn has influenced scientists for decades. It focuses on a progression of science involving periodic, fundamental shifts-revolutions-from one existing paradigm to another. Embedded in this theory is the concept of normal science, that is, scientists work within the confines of established theory, a process often compared to a type of puzzle-solving. This Kuhnian aspect of scientific research has received little attention relative to the much-scrutinized concepts of revolutions and paradigms. We use Kuhn's normal science framework to reflect on the way ecologists practice science. This involves a discussion of how theory dependence influences each step of the scientific method, specifically, how past experiences and existing research frameworks guide the way ecologists acquire knowledge. We illustrate these concepts with ecological examples, including food web structure and the biodiversity crisis, emphasizing that the way one views the world influences how that person engages in scientific research. We conclude with a discussion of how Kuhnian ideas inform ecological research at practical levels, such as influences on grant funding allocation, and we make a renewed call for the inclusion of philosophical foundations of ecological principles in pedagogy. By studying the processes and traditions of how science is carried out, ecologists can better direct scientific insight to address the world's most pressing environmental problems.

Leveraging green infrastructure for efficient treatment of reclaimed water.

Global water scarcity necessitates creative, yet practical, solutions to meet ever-growing demand. Green infrastructure is increasingly used in this context to provide water in environmentally friendly and sustainable ways. In this study, we focused on reclaimed wastewater from a joint gray and green infrastructure system employed by the Loxahatchee River District in Florida. The water system consists of a series of treatment stages for which we assessed 12 years of monitoring data. We measured water quality after secondary (gray) treatment, then in onsite lakes, offsite lakes, landscape irrigation (via sprinklers), and ultimately in downstream canals. Our findings show gray infrastructure designed for secondary treatment, integrated with green infrastructure, achieved nutrient concentrations nearly equivalent to advanced wastewater treatment systems. For example, we observed a dramatic decline in mean nitrogen concentration from 19.42 mg L-1 after secondary treatment to 5.26 mg L-1 after spending an average of 30 days in the onsite lakes. Nitrogen concentration continued to decline as reclaimed water moved from onsite lakes to offsite lakes (3.87 mg L-1) and irrigation sprinklers (3.27 mg L-1). Phosphorus concentrations exhibited a similar pattern. These decreasing nutrient concentrations led to relatively low nutrient loading rates and occurred while consuming substantially less energy and producing fewer greenhouse gas emissions than traditional gray infrastructure-at lower cost and higher efficiency. There was no evidence of eutrophication in canals downstream of the residential landscape whose sole source of irrigation water was reclaimed water. This study provides a long-term example of how circularity in water use can be used to work toward sustainable development goals.

Taxonomic identity best explains variation in body nutrient stoichiometry in a diverse marine animal community.

Animal-mediated nutrient dynamics are critical processes in ecosystems. Previous research has found animal-mediated nutrient supply (excretion) to be highly predictable based on allometric scaling, but similar efforts to find universal predictive relationships for an organism's body nutrient content have been inconclusive. We use a large dataset from a diverse tropical marine community to test three frameworks for predicting body nutrient content. We show that body nutrient content does not follow allometric scaling laws and that it is not well explained by trophic status. Instead, we find strong support for taxonomic identity (particularly at the family level) as a predictor of body nutrient content, indicating that evolutionary history plays a crucial role in determining an organism's composition. We further find that nutrients are "stoichiometrically linked" (e.g., %C predicts %N), but that the direction of these relationships does not always conform to expectations, especially for invertebrates. Our findings demonstrate that taxonomic identity, not trophic status or body size, is the best baseline from which to predict organismal body nutrient content.

Individual behavior drives ecosystem function and the impacts of harvest.

Current approaches for biodiversity conservation and management focus on sustaining high levels of diversity among species to maintain ecosystem function. We show that the diversity among individuals within a single population drives function at the ecosystem scale. Specifically, nutrient supply from individual fish differs from the population average >80% of the time, and accounting for this individual variation nearly doubles estimates of nutrients supplied to the ecosystem. We test how management (i.e., selective harvest regimes) can alter ecosystem function and find that strategies targeting more active individuals reduce nutrient supply to the ecosystem up to 69%, a greater effect than body size-selective or nonselective harvest. Findings show that movement behavior at the scale of the individual can have crucial repercussions for the functioning of an entire ecosystem, proving an important challenge to the species-centric definition of biodiversity if the conservation and management of ecosystem function is a primary goal.

Anthropogenic versus fish-derived nutrient effects on seagrass community structure and function.

Humans are altering nutrient dynamics through myriad pathways globally. Concurrent with the addition of nutrients via municipal, industrial, and agricultural sources, widespread consumer exploitation is changing consumer-mediated nutrient dynamics drastically. Thus, altered nutrient dynamics can occur through changes in the supply of multiple nutrients, as well as through changes in the sources of these nutrients. Seagrass ecosystems are heavily impacted by human activities, with highly altered nutrient dynamics from multiple causes. We simulate scenarios of altered nutrient supply and ratios, nitrogen:phosphorus (N:P), from two nutrient sources in seagrass ecosystems: anthropogenic fertilizer and fish excretion. In doing so we tested expectations rooted in ecological theory that suggest the importance of resource dynamics for predicting primary producer dynamics. Ecosystem functions were strongly altered by artificial fertilizer (e.g., seagrass growth increased by as much as 140%), whereas plant/algae community structure was most affected by fish-mediated nutrients or the interaction of both treatments (e.g., evenness increased by ~140% under conditions of low fish nutrients and high anthropogenic nutrients). Interactions between the nutrient sources were found for only two of six response variables, and the ratio of nutrient supply was the best predictor for only one response. These findings show that seagrass structure and function are well predicted by supply of a single nutrient (either N or P). Importantly, no single nutrient best explained the majority of responses-measures of community structure were best explained by the primary limiting nutrient to this system (P), whereas measures of growth and density of the dominant producer in the system were best explained by N. Thus, while our findings support aspects of theoretical expectations, the complexity of producer community responses belies broad generalities, underscoring the need to manage for multiple simultaneous nutrients in these imperiled coastal ecosystems.

Dissolved organic carbon and unimodal variation in sexual signal coloration in mosquitofish: a role for light limitation?

Natural selection plays an important role in the evolution of sexual communication systems. Here, we assess the effect of two well-known selection agents, transmission environment and predation, on interpopulation variation in sexual signals. Our model system is a series of 21 populations of Bahamian mosquitofish subjected to independent variation in optical conditions and predation risk. We show that optically diverse environments, caused by locally variable dissolved organic carbon concentrations, rather than spatial variation in predation, drove divergence in fin coloration (fin redness). We found a unimodal pattern of phenotypic variation along the optical gradient indicating a threshold-type response of visual signals to broad variation in optical conditions. We discuss evolutionary and ecological mechanisms that may drive such a pattern as well as the implications of non-monotonic clines for evolutionary differentiation.

Habitat fragmentation has some impacts on aspects of ecosystem functioning in a sub-tropical seagrass bed.

Habitat fragmentation impacts ecosystem functioning in many ways, including reducing the availability of suitable habitat for animals and altering resource dynamics. Fragmentation in seagrass ecosystems caused by propeller scarring is a major source of habitat loss, but little is known about how scars impact ecosystem functioning. Propeller scars were simulated in seagrass beds of Abaco, Bahamas, to explore potential impacts. To determine if plant-herbivore interactions were altered by fragmentation, amphipod grazers were excluded from half the experimental plots, and epiphyte biomass and community composition were compared between grazer control and exclusion plots. We found a shift from light limitation to phosphorus limitation at seagrass patch edges. Fragmentation did not impact top-down control on epiphyte biomass or community composition, despite reduced amphipod density in fragmented habitats. Seagrass and amphipod responses to propeller scarring suggest that severely scarred seagrass beds could be subject to changes in internal nutrient stores and amphipod distribution.

Animal pee in the sea: consumer-mediated nutrient dynamics in the world's changing oceans.

Humans have drastically altered the abundance of animals in marine ecosystems via exploitation. Reduced abundance can destabilize food webs, leading to cascading indirect effects that dramatically reorganize community structure and shift ecosystem function. However, the additional implications of these top-down changes for biogeochemical cycles via consumer-mediated nutrient dynamics (CND) are often overlooked in marine systems, particularly in coastal areas. Here, we review research that underscores the importance of this bottom-up control at local, regional, and global scales in coastal marine ecosystems, and the potential implications of anthropogenic change to fundamentally alter these processes. We focus attention on the two primary ways consumers affect nutrient dynamics, with emphasis on implications for the nutrient capacity of ecosystems: (1) the storage and retention of nutrients in biomass, and (2) the supply of nutrients via excretion and egestion. Nutrient storage in consumer biomass may be especially important in many marine ecosystems because consumers, as opposed to producers, often dominate organismal biomass. As for nutrient supply, we emphasize how consumers enhance primary production through both press and pulse dynamics. Looking forward, we explore the importance of CDN for improving theory (e.g., ecological stoichiometry, metabolic theory, and biodiversity-ecosystem function relationships), all in the context of global environmental change. Increasing research focus on CND will likely transform our perspectives on how consumers affect the functioning of marine ecosystems.

Fishing down nutrients on coral reefs.

Fishing is widely considered a leading cause of biodiversity loss in marine environments, but the potential effect on ecosystem processes, such as nutrient fluxes, is less explored. Here, we test how fishing on Caribbean coral reefs influences biodiversity and ecosystem functions provided by the fish community, that is, fish-mediated nutrient capacity. Specifically, we modelled five processes of nutrient storage (in biomass) and supply (via excretion) of nutrients, as well as a measure of their multifunctionality, onto 143 species of coral reef fishes across 110 coral reef fish communities. These communities span a gradient from extreme fishing pressure to protected areas with little to no fishing. We find that in fished sites fish-mediated nutrient capacity is reduced almost 50%, despite no substantial changes in the number of species. Instead, changes in community size and trophic structure were the primary cause of shifts in ecosystem function. These findings suggest that a broader perspective that incorporates predictable impacts of fishing pressure on ecosystem function is imperative for effective coral reef conservation and management.

Interpopulation Variation in a Condition-Dependent Signal: Predation Regime Affects Signal Intensity and Reliability.

In many models of sexual selection, conspicuous ornaments are preferred by mates because they indicate heritable signaler viability. To function as indicators, ornaments must exhibit a proportional relationship between expression and viability. In cases where the evolutionary interests of signaler and receiver diverge, selection favors exploitative exaggeration by low-viability individuals producing unreliable signals. Theory suggests that the evolutionary stability of such communication systems requires costs that prevent low-viability males from expressing disproportionately intense signals. Therefore, given ecological variation in signaling cost, the reliability of signaling systems will vary concomitantly. In this study, we assess the effect of a variable signal cost, predation, on signal intensity and reliability among 16 populations of Bahamas mosquitofish (Gambusia hubbsi) that use colorful dorsal fins in courtship displays. We found that fin coloration was more intense in low-predation sites and could be used to predict body condition. However, this predictive relationship was apparent only in populations subject to predation risk. We demonstrate an important role for ecological signaling cost in communication and show that ecological heterogeneity drives interpopulation variation in both the intensity and the reliability of a sexual signal.

Anthropogenic ecosystem fragmentation drives shared and unique patterns of sexual signal divergence among three species of Bahamian mosquitofish.

When confronted with similar environmental challenges, different organisms can exhibit dissimilar phenotypic responses. Therefore, understanding patterns of phenotypic divergence for closely related species requires considering distinct evolutionary histories. Here, we investigated how a common form of human-induced environmental alteration, habitat fragmentation, may drive phenotypic divergence among three closely related species of Bahamian mosquitofish (Gambusia spp.). Focusing on one phenotypic trait (male coloration), having a priori predictions of divergence, we tested whether populations persisting in fragmented habitats differed from those inhabiting unfragmented habitats and examined the consistency of the pattern across species. Species exhibited both shared and unique patterns of phenotypic divergence between the two types of habitats, with shared patterns representing the stronger effect. For all species, populations in fragmented habitats had fewer dorsal-fin spots. In contrast, the magnitude and trajectory of divergence in dorsal-fin color, a sexually selected trait, differed among species. We identified fragmentation-mediated increased turbidity as a possible driver of these trait shifts. These results suggest that even closely related species can exhibit diverse phenotypic responses when encountering similar human-mediated selection regimes. This element of unpredictability complicates forecasting the phenotypic responses of wild organisms faced with anthropogenic change - an important component of biological conservation and ecosystem management.

Rapid human-induced divergence of life-history strategies in Bahamian livebearing fishes (family Poeciliidae).

Human-induced rapid environmental change (HIREC) can have dramatic impacts on ecosystems, leading to rapid trait changes in some organisms and extinction in others. Such changes in traits signify that human actions can lead to cases of increased phenotypic diversity and consequently can strongly impact population-, community- and ecosystem-level dynamics. Here, we examine whether the ecological consequences of habitat fragmentation have led to changes in the life histories of three native species of mosquitofish (Gambusia spp.) inhabiting tidal creeks on six different Bahamian islands. We address two important questions: (i) How predictable and parallel are life-history changes in response to HIREC across islands and species, and (ii) what is the relative importance of shared (i.e. parallel) responses to fragmentation, differences between species or islands and species- or island-specific responses to fragmentation? Phenotypic differences between fragmentation regimes were as great or greater than differences between species or islands. While some adult life histories (lean weight and fat content) showed strong, shared responses to fragmentation, offspring-related life histories (embryo fat and fecundity) exhibited idiosyncratic, island-specific responses. While shared responses to fragmentation appeared largely driven by a reduction in piscivorous fish density, increased conspecific density and changes in salinity, we found some evidence that among-population variation in male reproductive investment and embryo fat content may have arisen via variation in conspecific density. Our results suggest that phenotypic responses to HIREC can be complex, with the predictability of response varying across traits. We therefore emphasize the need for more theoretical and empirical work to better understand the predictability of phenotypic responses to human-induced disturbances.

Metabolic theory and taxonomic identity predict nutrient recycling in a diverse food web.

Reconciling the degree to which ecological processes are generalizable among taxa and ecosystems, or contingent on the identity of interacting species, remains a critical challenge in ecology. Ecological stoichiometry (EST) and metabolic theory of ecology (MTE) are theoretical approaches used to evaluate how consumers mediate nutrient dynamics and energy flow through ecosystems. Recent theoretical work has explored the utility of these theories, but empirical tests in species-rich ecological communities remain scarce. Here we use an unprecedented dataset collected from fishes and dominant invertebrates (n = 900) in a diverse subtropical coastal marine community (50 families, 72 genera, 102 species; body mass range: 0.04-2,597 g) to test the utility of EST and MTE in predicting excretion rates of nitrogen (E(N)), phosphorus (E(P)), and their ratio (E(NP)). Body mass explained a large amount of the variation in EN and EP but not E(NP). Strong evidence in support of the MTE 3/4 allometric scaling coefficient was found for E(P), and for E(N) only after accounting for variation in excretion rates among taxa. In all cases, including taxonomy in models substantially improved model performance, highlighting the importance of species identity for this ecosystem function. Body nutrient content and trophic position explained little of the variation in E(N), E(P), or E(NP), indicating limited applicability of basic predictors of EST. These results highlight the overriding importance of MTE for predicting nutrient flow through organisms, but emphasize that these relationships still fall short of explaining the unique effects certain species can have on ecological processes.

Measuring individuality in habitat use across complex landscapes: approaches, constraints, and implications for assessing resource specialization.

Many mobile marine species are presumed to utilize a broad spectrum of habitats, but this seemingly generalist life history may arise from conspecifics specializing on distinct habitat alternatives to exploit foraging, resting/refuge, or reproductive opportunities. We acoustically tagged 34 red drum, and mapped sand, seagrass, marsh, or oyster (across discrete landscape contexts) use by each uniquely coded individual. Using 144,000 acoustic detections, we recorded differences in habitat use among red drum: proportional use of seagrass habitat ranged from 0 to 100%, and use of oyster-bottom types also varied among fish. WIC/TNW and IS metrics (previously applied vis-à-vis diet specialization) consistently indicated that a typical red drum overlapped >70% with population-level niche exploitation. Monte Carlo permutations showed these values were lower than expected had fish drawn from a common habitat-use distribution, but longitudinal comparisons did not provide evidence of temporally consistent individuality, suggesting that differences among individuals were plastic and not reflective of true specialization. Given the range of acoustic detections we captured (from tens to 1,000s per individual), which are substantially larger sample sizes than in many diet studies, we extended our findings by serially reducing or expanding our data in simulations to evaluate sample-size effects. We found that the results of null hypothesis testing for specialization were highly dependent on sample size, with thresholds in the relationship between sample size and associated P-values. These results highlight opportunities and potential caveats in exploring individuality in habitat use. More broadly, exploring individual specialization in fine-scale habitat use suggests that, for mobile marine species, movement behaviors over shorter (≤weeks), but not longer (≥months), timescales may serve as an underlying mechanism for other forms of resource specialization.

Size, sex and individual-level behaviour drive intrapopulation variation in cross-ecosystem foraging of a top-predator.

Large-bodied, top-predators are often highly mobile, with the potential to provide important linkages between spatially distinct food webs. What biological factors contribute to variation in cross-ecosystem movements, however, have rarely been examined. Here, we investigated how ontogeny (body size), sex and individual-level behaviour impacts intrapopulation variation in cross-ecosystem foraging (i.e. between freshwater and marine systems), by the top-predator Alligator mississippiensis. Field surveys revealed A. mississippiensis uses marine ecosystems regularly and are abundant in estuarine tidal creeks (from 0·3 to 6·3 individuals per km of creek, n = 45 surveys). Alligator mississippiensis captured in marine/estuarine habitats were significantly larger than individuals captured in freshwater and intermediate habitats. Stomach content analysis (SCA) showed that small juveniles consumed marine/estuarine prey less frequently (6·7% of individuals) than did large juveniles (57·8%), subadult (73%), and adult (78%) size classes. Isotopic mixing model analysis (SIAR) also suggests substantial variation in use of marine/estuarine prey resources with differences among and within size classes between sexes and individuals (range of median estimates for marine/estuarine diet contribution = 0·05-0·76). These results demonstrate the importance of intrapopulation characteristics (body size, sex and individual specialization) as key determinants of the strength of predator-driven ecosystem connectivity resulting from cross-ecosystem foraging behaviours. Understanding the factors, which contribute to variation in cross-ecosystem foraging behaviours, will improve our predictive understanding of the effects of top-predators on community structure and ecosystem function.

Ecosystem fragmentation drives increased diet variation in an endemic livebearing fish of the Bahamas.

One consequence of human-driven habitat degradation in general, and habitat fragmentation in particular, is loss of biodiversity. An often-underappreciated aspect of habitat fragmentation relates to changes in the ecology of species that persist in altered habitats. In Bahamian wetlands, ecosystem fragmentation causes disruption of hydrological connectivity between inland fragmented wetlands and adjacent marine areas, with the consequent loss of marine piscivores from fragmented sections. We took advantage of this environmental gradient to investigate effects of ecosystem fragmentation on patterns of resource use in the livebearing fish Gambusia hubbsi (Family Poeciliidae), using both population- and individual-level perspectives. We show that fragmentation-induced release from predation led to increased G. hubbsi population densities, which consequently led to lower mean growth rates, likely as a result of higher intraspecific competition for food. This was accompanied by a broadening of dietary niches via increased interindividual diet variation, suggesting a negative effect of predation and a positive effect of intraspecific competition on the degree of diet variation in natural populations. Our results therefore indicate that habitat fragmentation can greatly impact the ecology of resilient populations, with potentially important ecological and evolutionary implications.

Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems.

Corals thrive in low nutrient environments and the conservation of these globally imperiled ecosystems is largely dependent on mitigating the effects of anthropogenic nutrient enrichment. However, to better understand the implications of anthropogenic nutrients requires a heightened understanding of baseline nutrient dynamics within these ecosystems. Here, we provide a novel perspective on coral reef nutrient dynamics by examining the role of fish communities in the supply and storage of nitrogen (N) and phosphorus (P). We quantified fish-mediated nutrient storage and supply for 144 species and modeled these data onto 172 fish communities (71 729 individual fish), in four types of coral reefs, as well as seagrass and mangrove ecosystems, throughout the Northern Antilles. Fish communities supplied and stored large quantities of nutrients, with rates varying among ecosystem types. The size structure and diversity of the fish communities best predicted N and P supply and storage and N : P supply, suggesting that alterations to fish communities (e.g., overfishing) will have important implications for nutrient dynamics in these systems. The stoichiometric ratio (N : P) for storage in fish mass (~8 : 1) and supply (~20 : 1) was notably consistent across the four coral reef types (but not seagrass or mangrove ecosystems). Published nutrient enrichment studies on corals show that deviations from this N : P supply ratio may be associated with poor coral fitness, providing qualitative support for the hypothesis that corals and their symbionts may be adapted to specific ratios of nutrient supply. Consumer nutrient stoichiometry provides a baseline from which to better understand nutrient dynamics in coral reef and other coastal ecosystems, information that is greatly needed if we are to implement more effective measures to ensure the future health of the world's oceans.

Does landscape context mediate the nature of density dependence for a coral reef fish?

Over-harvest and landscape change are two of the greatest threats to marine ecosystems. Over-harvest may directly affect key population regulation mechanisms (e.g., density dependence), with the magnitude of the effects being further influenced by changes in landscape structure and associated resource availability. Because resource availability and conspecific density often co-vary within the natural landscape, manipulative experiments are needed to understand how changes in these two drivers may affect density dependence in wild populations. We used a common, shoaling, coral reef fish (white grunt, Haemulon plumierii) as our model species, and manipulated fish densities and landscape context of artificial reef habitats to assess the effects of each on fish condition. We found evidence of inverse density dependence, where individual condition was positively related to conspecific density; landscape context had little effect. Mean grunt condition on natural patch reefs was similar to that for our low grunt density treatment artificial reefs, possibly due to differences in fish densities or landscape context. These findings suggest that over-harvest may have detrimental effects on wild populations that extend beyond mere reductions in population size, especially for group-living species.

Human-caused habitat fragmentation can drive rapid divergence of male genitalia.

The aim of this study rests on three premises: (i) humans are altering ecosystems worldwide, (ii) environmental variation often influences the strength and nature of sexual selection, and (iii) sexual selection is largely responsible for rapid and divergent evolution of male genitalia. While each of these assertions has strong empirical support, no study has yet investigated their logical conclusion that human impacts on the environment might commonly drive rapid diversification of male genital morphology. We tested whether anthropogenic habitat fragmentation has resulted in rapid changes in the size, allometry, shape, and meristics of male genitalia in three native species of livebearing fishes (genus: Gambusia) inhabiting tidal creeks across six Bahamian islands. We found that genital shape and allometry consistently and repeatedly diverged in fragmented systems across all species and islands. Using a model selection framework, we identified three ecological consequences of fragmentation that apparently underlie observed morphological patterns: decreased predatory fish density, increased conspecific density, and reduced salinity. Our results demonstrate that human modifications to the environment can drive rapid and predictable divergence in male genitalia. Given the ubiquity of anthropogenic impacts on the environment, future research should evaluate the generality of our findings and potential consequences for reproductive isolation.