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The effects of overdispersion and zero inflation (e.g., poor model fits) can result in misinterpretation in studies using count data. These effects have not been evaluated in paleoecological studies of predation and are further complicated by preservational bias and time averaging. We develop a hierarchical Bayesian framework to account for uncertainty from overdispersion and zero inflation in estimates of specimen and predation trace counts. We demonstrate its application using published data on drilling predators and their prey in time-averaged death assemblages from the Great Barrier Reef, Australia.
Our results indicate that estimates of predation frequencies are underestimated when zero inflation is not considered, and this effect is likely compounded by removal of individuals and predation traces via preservational bias. Time averaging likely reduces zero inflation via accumulation of rare taxa and events; however, it increases the uncertainty in comparisons between assemblages by introducing variability in sampling effort. That is, there is an analytical cost with time-averaged count data, manifesting as broader confidence regions. Ecological inferences in paleoecology can be strengthened by accounting for the uncertainty inherent to paleoecological count data and the sampling processes by which they are generated.
As the climate changes and ecosystems shift toward novel combinations of species, the methods and metrics of conservation science are becoming less species-centric. To meet this growing need, marine conservation paleobiologists stand to benefit from the addition of new, taxon-free benthic indices to the live–dead analysis tool kit. These indices, which were developed to provide actionable, policy-specific data, can be applied to the readily preservable component of benthic communities (e.g., mollusks) to assess the ecological quality status of the entire community. Because these indices are taxon-free, they remain applicable even as the climate changes and novel communities develop—making them a potentially valuable complement to traditionally applied approaches for live–dead analysis, which tend to focus on maintaining specific combinations of species under relatively stable environmental conditions. Integrating geohistorical data with these established indices has potential to increase the salience of the live–dead approach in the eyes of resource managers and other stakeholders.
Site-selectivity analysis of drilling predation traces may provide useful behavioral information concerning a predator interacting with its prey. However, traditional approaches exclude some spatial information (i.e., oversimplified trace position) and are dependent on the scale of analysis (e.g., arbitrary grid system used to divide the prey skeleton into sectors). Here we introduce the spatial point pattern analysis of traces (SPPAT), an approach for visualizing and quantifying the distribution of traces on shelled invertebrate prey, which includes improved collection of spatial information inherent to drillhole location (morphometric-based estimation), improved visualization of spatial trends (kernel density and hotspot mapping), and distance-based statistics for hypothesis testing (K-, L-, and pair correlation functions). We illustrate the SPPAT approach through case studies of fossil samples, modern beach-collected samples, and laboratory feeding trials of naticid gastropod predation on bivalve prey. Overall results show that kernel density and hotspot maps enable visualization of subtle variations in regions of the shell with higher density of predation traces, which can be combined with the maximum clustering distance metric to generate hypotheses on predatory behavior and anti-predatory responses of prey across time and geographic space. Distance-based statistics also capture the major features in the distribution of traces across the prey skeleton, including aggregated and segregated clusters, likely associated with different combinations of two modes of drilling predation, edge and wall drilling. The SPPAT approach is transferable to other paleoecologic and taphonomic data such as encrustation and bioerosion, allowing for standardized investigation of a wide range of biotic interactions.
Life span bias potentially alters species abundance in death assemblages through the overrepresentation of short-lived organisms compared with their long-lived counterparts. Although previous work found that life span bias did not contribute significantly to live–dead discordance in bivalve assemblages, life span bias better explained discordance in two groups: longer-lived bivalve species and species with known life spans. More studies using local, rather than global, species-wide life spans and mortality rates would help to determine the prevalence of life span bias, especially for long-lived species with known life spans. Here, we conducted a field study at two sites in North Carolina to assess potential life span bias between Mercenaria mercenaria and Chione elevata, two long-lived bivalve species that can be aged directly. We compared the ability of directly measured local life spans with that of regional and global life spans to predict live–dead discordance between these two species. The shorter-lived species (C. elevata) was overrepresented in the death assemblage compared with its live abundance, and local life span data largely predicted the amount of live–dead discordance; local life spans predicted 43% to 88% of discordance. Furthermore, the global maximum life span for M. mercenaria resulted in substantial overpredictions of discordance (1.4 to 1.6 times the observed live–dead discordance). The results of this study suggest that life span bias should be considered as a factor affecting proportional abundances of species in death assemblages and that using life span estimates appropriate to the study locality improves predictions of discordance based on life span compared with using global life span estimates.
Where do species that become important players in ecosystems evolve? This simple yet crucial question must be answered if we want to understand how the biosphere is rejuvenated following a crisis. We cannot simply assume that the environments in which we find fossil remains of a given species, or living populations of a species, are the environments in which that species evolved. Take the most obvious example: Fossil human skeletons have been unearthed by the hundreds in North America, but all available evidence points to a human origin in Africa. We can often identify the general geographic origins of species and clades thanks to fossil occurrences and the application of phylogenetic techniques; but can we do likewise for more ecological aspects of the environment? Advances in population biology and in paleobiology now permit us to outline a hypothesis of the circumstances most favorable to the evolution of abundant, widespread, or ecologically powerful species, those with adaptations that are selectively advantageous across many environments, and large short-term and long-term effects in ecosystems.
More than 1600 valves of Late Cretaceous and early Paleocene Northern Atlantic Coastal Plain gryphaeid oysters (Exogyrinae and Pycnodonteinae) were examined for breakage-induced shell repair and morphologic variability to evaluate the hypothesis of escalation. The Exogyrinae show disproportionately higher average repair frequency (0.41) relative to the ecologically and functionally similar unornamented pycnodonts (0.19). An increase in repair frequency (independent evidence of the action of a selective agent, e.g., predation) through the stratigraphic interval supports escalation. Variation in repair frequencies may reflect differences in oyster morphology and in the strength and diversity of shell crushers across an onshore-offshore gradient. Escalation of antipredatory adaptation characterized the evolutionary response of gryphaeid oysters to their durophagous predators. Adaptation generally occurred by the enhancement of existing traits in both oyster lineages. Characters that confer a selective advantage against predators are not all expressed or improved concurrently in both oyster lineages. Morphologic adaptations to minimize shell breakage include the development of expansive, broad commissural shelves, thickened valves, and surface ornamentation (Exogyrinae). Surface ornament in the Exogyrinae gradually increased with time. For some characters, such as thickness, conflicting functional demands (e.g., valve stabilization) may have limited adaptation to predators.
Drillholes made by naticid and muricid gastropods are frequently used in evolutionary and ecological studies because they provide direct, preservable evidence of predation. The muricid Ecphora is common in many Neogene Atlantic Coastal Plain assemblages in the United States, but is frequently ignored in studies of naticid predation. We used a combination of Pliocene fossil, modern beach, and experimentally derived samples to evaluate the hypothesis that Ecphora was an important source of drillholes in infaunal bivalve prey shared with naticids. We focused on the large, thick-shelled venerid, Mercenaria, which is commonly drilled by naticids today. Laboratory experiments, modern beach samples, and the published literature confirm that naticids preferentially drill near the umbo (significant clumping of holes), show a significant correlation between prey size and predator size (estimated by outer borehole diameter), and prefer Mercenaria <50 mm antero-posterior width when other prey are present. Fossil samples containing Ecphora (with or without other large muricids) show no drillhole site stereotypy (no significant clumping, greater variability in placement), no significant predator: prey size correlation, drilled prey shells larger than the largest modern naticids could produce in an experimental setting, and drillholes larger in diameter than those estimated for the largest Pliocene naticids, thus supporting our hypothesis. Substantial overlap in the placement of holes drilled by naticids and muricids, however, made identifying predators from drillhole position problematic. The lack of overlapping ranges of prey shell thickness between fossil and other samples precluded the use of drillhole morphology to establish predator identity (e.g., ratio of inner borehole diameter to outer borehole diameter, drillhole angle). Whereas the difficulty in determining predator identity from drillholes limits the types of analyses that can be reliably performed in mixed-predator assemblages, recognizing Ecphora as a prominent drilling predator creates the opportunity to investigate previously unrecognized questions.
An outstanding challenge with broad implications for an ecologically sustainable future is to understand how living systems—whether natural or social—balance opportunity and constraint in a given environment. In this paper, I compare the proposed mechanics of a heuristic developed to explain transformational change in systems ecology with various paleontological patterns and hypotheses for its conceptual homology and thus explanatory power in causal terms. The adaptive cycle heuristic, which has potential to influence current environmental and natural resources law and policy, has two components: 1) cycles that alternate between long periods of growth and shorter periods that create opportunities for innovation (new structures or conditions that become economically successful), and 2) the interaction of nested sets of such cycles (panarchies) across space and time scales. I critically evaluate three basic underlying tenets of the adaptive cycle related to the circumstances of innovation—empty niche space, competition and availability of resources—because of their importance to the development of a theoretical framework for understanding the ecological dimension of opportunity in biological evolution. I conclude that not all of the proposed mechanics and observed phenomenology of the adaptive cycle are appropriate in biological evolution. I draw insight, however, from the hierarchical nature of the heuristic to outline a “panarchical” conceptualization of the escalation hypothesis; I identify self-organization, emergence, selection and adaptation, and feedback as phenomena that are held in common across systems and scales, which influence how entities in the economic hierarchy of life arise, interact and evolve.
Two roads diverged in a wood, and I, I took the one less traveled by, and that has made all the difference. Robert Frost.
Every system either finds a way to develop or else collapses. Aleksander Solzhenitsyn
Edge drilling is a form of predation in which a predatory snail excavates a hole at a point along the margin of the closed valves of a bivalved animal. We tested the hypothesis that edge-drilling attacks by the predatory snail Chicoreus dilectus on its clam prey Chione elevata shorten the duration of the predation process relative to the alternative behaviour of drilling through the prey's shell wall away from its edges. The time required to complete an edge-drilling attack was on average about three times less than when prey were attacked through the shell wall. This improvement in predation speed was a function of the thickness of the prey's shell at the point of attack. We suggest that owing to the shorter length of time required to kill prey, the edge-drilling behaviour may be selectively advantageous in environments where enemies are abundant, especially competitors that might attempt to steal prey. Behaviours that speed up the predation process may create opportunities for more effective exploitation of available prey resources in highly competitive environments.
Arms races between predators and prey may be driven by two related processes—escalation and coevolution. Escalation is enemy-driven evolution. In this top-down view of an arms race, the role of prey (with the exception of dangerous prey) is downplayed. In coevolution, two or more species change reciprocally in response to one another; prey are thought to drive the evolution of their predator, and vice versa. In the fossil record, the two processes are most reliably distinguished when the predator-prey system is viewed within the context of the other species that may influence the interaction, thus allowing for a relative ranking of the importance of selective agents. Detailed documentation of the natural history of living predator-prey systems is recommended in order to distinguish the processes in some fossil systems. A geographic view of species interactions and the processes driving their evolution may lead to a more diverse array of testable hypotheses on how predator-prey systems evolve and what constraints interactions impose on the evolution of organisms. Scale is important in evaluating the role of escalation and coevolution in the evolution of species interactions. If short-term reciprocal adaptation (via phenotypic plasticity or selection mosaics among populations) between predator and prey is a common process, then prey are likely to exert some selective pressure over their predators over the short term (on ecological time scales), but in the long run predators may still exert primary “top-down” control in directing evolution. On the scale of evolutionary time, predators of large effect likely control the overall directionality of evolution due to the inequalities of predator and prey in control of resources.
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