The Hierarchy-of-Hypotheses Approach: A Synthesis Method for Enhancing Theory Development in Ecology and Evolution.

In the current era of Big Data, existing synthesis tools such as formal meta-analyses are critical means to handle the deluge of information. However, there is a need for complementary tools that help to (a) organize evidence, (b) organize theory, and (c) closely connect evidence to theory. We present the hierarchy-of-hypotheses (HoH) approach to address these issues. In an HoH, hypotheses are conceptually and visually structured in a hierarchically nested way where the lower branches can be directly connected to empirical results. Used for organizing evidence, this tool allows researchers to conceptually connect empirical results derived through diverse approaches and to reveal under which circumstances hypotheses are applicable. Used for organizing theory, it allows researchers to uncover mechanistic components of hypotheses and previously neglected conceptual connections. In the present article, we offer guidance on how to build an HoH, provide examples from population and evolutionary biology and propose terminological clarifications.

Effects of dams on downstream molluscan predator-prey interactions in the Colorado River estuary.

River systems worldwide have been modified for human use and the downstream ecological consequences are often poorly understood. In the Colorado River estuary, where upstream water diversions have limited freshwater input during the last century, mollusc remains from the last several hundred years suggest widespread ecological change. The once abundant clam Mulinia modesta has undergone population declines of approximately 94% and populations of predators relying on this species as a food source have probably declined, switched to alternative prey species or both. We distinguish between the first two hypotheses using a null model of predation preference to test whether M. modesta was preyed upon selectively by the naticid snail, Neverita reclusiana, along the estuary's past salinity gradient. To evaluate the third hypothesis, we estimate available prey biomass today and in the past, assuming prey were a limiting resource. Data on the frequency of drill holes-identifiable traces of naticid predation on prey shells-showed several species, including M. modesta, were preferred prey. Neverita reclusiana was probably able to switch prey. Available prey biomass also declined, suggesting the N. reclusiana population probably also declined. These results indicate a substantial change to the structure of the benthic food web. Given the global scale of water management, such changes have probably also occurred in many of the world's estuaries.

History matters: ecometrics and integrative climate change biology.

Climate change research is increasingly focusing on the dynamics among species, ecosystems and climates. Better data about the historical behaviours of these dynamics are urgently needed. Such data are already available from ecology, archaeology, palaeontology and geology, but their integration into climate change research is hampered by differences in their temporal and geographical scales. One productive way to unite data across scales is the study of functional morphological traits, which can form a common denominator for studying interactions between species and climate across taxa, across ecosystems, across space and through time-an approach we call 'ecometrics'. The sampling methods that have become established in palaeontology to standardize over different scales can be synthesized with tools from community ecology and climate change biology to improve our understanding of the dynamics among species, ecosystems, climates and earth systems over time. Developing these approaches into an integrative climate change biology will help enrich our understanding of the changes our modern world is undergoing.

Conservation palaeobiology and the shape of things to come.

Conservation decision-making is a forward-looking process that involves choices among alternative images of how the future will unfold. Scenarios, easily understood as stories about plausible futures, are emerging as a powerful approach used by the conservation community to define a range of socio-ecological futures when standard, predictive modelling approaches to decision-making are inappropriate, providing a framework for making robust decisions under uncertainties. Conservation palaeobiologists can help the conservation community imagine the future. The utility of the past centres on orienting us to the present-grounding the future in the realm of what is plausible-by providing context against which to think about future scenarios, which may help stakeholders and decision-makers to develop a new mental map of a conservation problem, inspiring our intentions and moving us purposefully toward a desirable tomorrow. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

The trans-Atlantic history of diversity and body size in ecological guilds.

Geographically separate biotas often show differences in species composition, diversity, and adaptations. Such differences, which often reflect historical differences in regimes of productivity and selection, have received little attention from ecologists. Here we concentrate on diversity and maximum body size in 18 guilds of shallow-water marine shell-bearing mollusks and barnacles from the European and North American sides of the temperate North Atlantic. These guilds represent suspension-feeders (epifaunal, shallow infaunal, and deep infaunal), chemosymbiotic bivalves, predators, and grazers. Geographic patterns among Recent guilds were compared to those during Pliocene and early Miocene time in order to determine how diversity and maximum size changed over the last 17 million years in the face of high levels of extinction and species invasion. Recent European guilds are generally more diverse than their American counterparts, a finding consistent with previous biota-wide analyses. Diversity within Pliocene guilds was often higher on the American side, but this stems in part from the large subtropical component in preserved temperate Pliocene guilds in Virginia but not in Europe. The largest species in hard-bottom guilds in Europe reach greater sizes than those in comparable American guilds, but for sand-bottom guilds, American species almost always attain greater sizes than their European counterparts. These size differences have changed little since early Miocene time despite high levels of Pliocene and Pleistocene extinction in invasion, particularly on the American side. Large-bodied species are overrepresented among both extinct and invading lineages, meaning that lineage replacement has been the rule for the largest species in guilds on both sides of the Atlantic. Together with previous studies, these results may imply that sand-bottom environments in North America have been more productive and have experienced more far-reaching escalation between shell-bearing species and their predators than their European counterparts since early Miocene time. The Pliocene to Recent record of hard-bottom guilds implies that productivity and/or escalation in these systems may have been higher on the European side than in eastern North America. Shallow-water guilds on opposite sides of the Atlantic have retained differences despite great upheavals caused by extinctions and invasions during the last 3 million years.

Indirect effects of climate change altered the cannibalistic behaviour of shell-drilling gastropods in Antarctica during the Eocene.

The fossil record from Seymour Island, Antarctic Peninsula, provides a record of biotic response to the onset of global climatic cooling during the Eocene. Using drilling traces-small, round holes preserved on prey shells-we examined the effect of a cooling pulse 41 Ma on the cannibalistic behaviour of predatory naticid gastropods. We predicted that cannibalistic attacks would decline in response to the cooling climate, reflecting reduced activity levels, energy requirements and constraints on the chemically aided drilling process of the naticids. Surprisingly, however, cannibalism frequencies did not change. This counterintuitive result is best explained by a sharp reduction in durophagous (shell-crushing) predation in shallow-benthic communities in Antarctica that also occurred as the climate cooled. Reduced durophagous predation may have created a less-risky environment for foraging naticids, stimulating cannibalistic behaviour. The change in the top-down control exerted by shell-crushing predators on naticids may have counteracted the direct, negative effects of declining temperatures on the predatory performance of naticids. Our results suggest that the long-term consequences of climate change cannot be predicted solely from its direct effects on predation, because the temperature can have large indirect effects on consumer-resource interactions, especially where risk-effects dominate.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems.

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

Geohistorical records indicate no impact of the Deepwater Horizon oil spill on oyster body size.

Documentation of the near- and long-term effects of the Deepwater Horizon (DWH) oil spill, one of the largest environmental disasters in US history, is still ongoing. We used a novel before-after-control-impact analysis to test the hypothesis that average body size of intertidal populations of the eastern oyster (Crassostrea virginica) inhabiting impacted areas in Louisiana decreased due to increased stress/mortality related to the oil spill. Time-averaged death assemblages of oysters were used to establish a pre-spill baseline of body-size structure for four impacted and four control locations along a 350 km stretch of Louisiana's coastline. Post-spill body sizes were then measured from live oysters at each site in order to evaluate the differences in body size between oiled (i.e. impact) and unoiled (i.e. control) locations before and after the spill. Our results indicate that average body size of oysters remained relatively unchanged after the oil spill. There were also no temporal patterns in temperature, salinity or disease prevalence that could have explained our results. Together, these findings suggest that oysters either recovered rapidly following the immediate impact of the DWH oil spill, or that its impact was not severe enough to influence short-term population dynamics of the oyster beds.

Fossil clam shells reveal unintended carbon cycling consequences of Colorado River management.

Water management that alters riverine ecosystem processes has strongly influenced deltas and the people who depend on them, but a full accounting of the trade-offs is still emerging. Using palaeoecological data, we document a surprising biogeochemical consequence of water management in the Colorado River basin. Complete allocation and consumptive use of the river's flow has altered the downstream estuarine ecosystem, including the abundance and composition of the mollusc community, an important component in estuarine carbon cycling. In particular, population declines in the endemic Colorado delta clam, Mulinia coloradoensis, from 50--125 individuals m-2 in the pre-dam era to three individuals m-2 today, have likely resulted in a reduction, on the order of 5900-15 000 t C yr-1 (4.1-10.6 mol C m-2 yr-1), in the net carbon emissions associated with molluscs. Although this reduction is large within the estuarine system, it is small in comparison with annual global carbon emissions. Nonetheless, this finding highlights the need for further research into the effects of dams, diversions and reservoirs on the biogeochemistry of deltas and estuaries worldwide, underscoring a present need for integrated water and carbon planning.

Escalation and extinction selectivity: morphology versus isotopic reconstruction of bivalve metabolism.

Studies that have tested and failed to support the hypothesis that escalated species (e.g., those with predation-resistant adaptations) are more susceptible to elimination during mass extinctions have concentrated on the distribution and degree of morphological defenses in molluscan species. This morphological approach to determining level of escalation in bivalves may be oversimplified because it does not account for metabolic rate, which is an important measure of escalation that is less readily accessible for fossils. Shell growth rates in living bivalves are positively correlated with metabolic rate and thus are potential indicators of level of escalation. To evaluate this approach, we used oxygen isotopes to reconstruct shell growth rates for two bivalve species (Macrocallista marylandica and Glossus markoei) from Miocene-aged sediments of Maryland. Although both species are classified as non-escalated based on morphology, the isotopic data indicate that M. marylandica was a faster-growing species with a higher metabolic rate and G. markoei was a slower-growing species with a lower metabolic rate. Based on these results, we predict that some morphologically non-escalated species in previous tests of extinction selectivity should be reclassified as escalated because of their fast shell growth rates (i.e., high metabolic rates). Studies that evaluate the level of escalation of a fauna should take into account the energetic physiology of taxa to avoid misleading results.

Abundance is not enough: the need for multiple lines of evidence in testing for ecological stability in the fossil record.

The fossil record is the only source of information on the long-term dynamics of species assemblages. Here we assess the degree of ecological stability of the epifaunal pterioid bivalve assemblage (EPBA), which is part of the Middle Devonian Hamilton fauna of New York--the type example of the pattern of coordinated stasis, in which long intervals of faunal persistence are terminated by turnover events induced by environmental change. Previous studies have used changes in abundance structure within specific biofacies as evidence for a lack of ecological stability of the Hamilton fauna. By comparing data on relative abundance, body size, and predation, indexed as the frequency of unsuccessful shell-crushing attacks, of the EPBA, we show that abundance structure varied through time, but body-size structure and predation pressure remained relatively stable. We suggest that the energetic set-up of the Hamilton fauna's food web was able to accommodate changes in species attributes, such as fluctuating prey abundances. Ecological redundancy in prey resources, adaptive foraging of shell-crushing predators (arising from predator behavioral or adaptive switching in prey selection in response to changing prey abundances), and allometric scaling of predator-prey interactions are discussed as potential stabilizing factors contributing to the persistence of the Hamilton fauna's EPBA. Our study underscores the value and importance of multiple lines of evidence in tests of ecological stability in the fossil record.

Conservation paleobiology: putting the dead to work.

Geohistorical data and analyses are playing an increasingly important role in conservation biology practice and policy. In this review, we discuss examples of how the near-time and deep-time fossil record can be used to understand the ecological and evolutionary responses of species to changes in their environment. We show that beyond providing crucial baseline data, the conservation paleobiology perspective helps us to identify which species will be most vulnerable and what kinds of responses will be most common. We stress that inclusion of geohistorical data in our decision-making process provides a more scientifically robust basis for conservation policies than those dependent on short-term observations alone.

Specialized shell-breaking crab claws in Cretaceous seas.

Here we report on a large brachyuran crab species from the Late Cretaceous of Mexico that has claws indicative of highly specialized shell-breaking behaviour. This crab possessed dimorphic claws (the right larger than the left), armed with several broad teeth, including a curved tooth structure found at the base of the movable finger of the right claw. The curved tooth is similar to the one observed on claws of many living durophagous crabs that use it as a weapon to peel, crush or chip the edges of hard-shelled prey, particularly molluscs. These morphological traits suggest that specialized shell-breaking crab predators had evolved during the Cretaceous, which contradicts previous findings supporting an Early Cenozoic origin for specialized shell crushers within the brachyuran clade.

Crab scars reveal survival advantage of left-handed snails.

Biological asymmetries are important elements of the structure and function of many living organisms. Using the Plio-Pleistocene fossil record of crab predation on morphologically similar pairs of right- and left-handed snail species, we show here for the first time, contrary to traditional wisdom, that rare left-handed coiling promotes survival from attacks by right-handed crabs. This frequency-dependent result influences the balance of selection processes that maintain left-handedness at the species level and parallels some social interactions in human cultures, such as sports that involve dual contests between opponents of opposite handedness.

Comment on "Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates".

Madin et al. (Reports, 12 May 2006, p. 897) reported that escalation has not been an important cause of biological change throughout the history of life. However, they evaluated the escalation hypothesis with inappropriate data. First, global-scale data integrate heterogeneous signals that obscure the economic context of life. Second, diversity data cannot yield information about selection and adaptation.

Reduced competition and altered feeding behavior among marine snails after a mass extinction.

Extinction may alter competitive interactions among surviving species, affecting their subsequent recovery and evolution, but these processes remain poorly understood. Analysis of predation traces produced by shell-drilling muricid snails on bivalve prey reveals that species interactions were substantially different before and after a Plio-Pleistocene mass extinction in the western Atlantic. Muricids edge- and wall-drilled their prey in the Pliocene, but Pleistocene and Recent snails attacked prey only through the shell wall. Experiments with living animals suggest that intense competition induces muricid snails to attack shell edges. Pliocene predators, therefore, probably competed for resources more intensely than their post-extinction counterparts.