John Warren Huntley

Strong coupling of predation intensity and diversity in the Phanerozoic fossil record

The importance of ecological interactions in driving the evolution of animals has been the focus of intense debate among paleontologists, evolutionary biologists, and macroecologists. To test whether the intensity of such interactions covaries with the secular evolutionary trend in global biodiversity, we compiled a species-level database of predation intensity, as measured by the frequency of common predation traces (drillings and repair scars ranging in age from Ediacaran to Holocene). The results indicate that the frequency of predation traces increased notably by the Ordovician, and not in the mid-Paleozoic as suggested by multiple previous studies. Importantly, these estimates of predation intensity and global diversity of marine metazoans correlate throughout the Phanerozoic fossil record regardless of corrections and methods applied. This concordance may represent (i) an ecological signal: long-term coupling of diversity and predation; (ii) a diversity-driven diffusion of predatory behaviors: an increased probability of more complex predatory strategies to appear at higher diversity levels; or (iii) a spurious concordance in signal capture: an artifact where rare species and less-frequent (e.g., trace-producing) predatory behaviors are both more detectable at times when sampling improves. The coupling of predation and diversity records suggests that macroevolutionary and macroecological patterns share common causative mechanisms that may reflect either historical processes or sampling artifacts.

The latest Ediacaran Wormworld fauna: Setting the ecological stage for the Cambrian Explosion

This is the published version of an article published by the Geological Society of America.

Testing limiting similarity in Quaternary terrestrial gastropods

Abstract The hypothesis of limiting similarity, which postulates that morphologically and/or ecologically similar species will differ enough in shape, size, or other variables to minimize competition, has been controversial among ecologists and paleoecologists. Many studies have reported the occurrence of limiting similarity in modern environments or in time-averaged fossil deposits; however, empirical high-resolution time series demonstrating limiting similarity over longer time scales are lacking. We have integrated radiocarbon-calibrated amino acid dating techniques, stable isotope estimates, and morphometric data to test the hypothesis of limiting similarity in late Quaternary land snails from the Canary Islands over a period of 42,500 years. We tested for both ecological character displacement (two closely related species will differ in size in order to minimize competition in sympatry and these differences will be minimized in allopatry) and community-wide character displacement (overdispersion of body size among competitors in a guild). Multiple proxies of body size consistently show that two endemic congeneric pulmonate gastropod species (Theba geminata and T. arinagae) maintained a difference in size from ∼42,500 b.p. through the last occurrence of T. arinagae 14,900 b.p., with a concomitant trend of a decreasing body size. Theba geminata body size did not converge on that of T. arinagae and variation in T. geminata body size did not increase significantly following the extinction of T. arinagae; therefore, ecological character displacement and release did not occur. Community-wide character displacement was found in only one time bin over the last 42,500 years. These results suggest that limiting similarity is a transient ecological phenomenon rather than a long-term evolutionary process. This study not only demonstrates the problems inherent in biological “snapshot” studies and geological studies of time-averaged deposits to test limiting similarity adequately, but it also presents a more adequate research protocol to test the importance of interspecific competition in the history of life.

Evolutionary and ecological implications of trematode parasitism of modern and fossil northern Adriatic bivalves

Abstract The role of antagonistic organismal interactions in the production of long-term macroevolutionary trends has been debated for decades. Some evidence seems to suggest that temporal trends in predation frequency share a common causative mechanism with genus-level diversity, whereas studies on the role of parasites in “shaping” the evolutionary process are rare indeed. Digenean trematodes (Phylum Platyhelminthes) infest molluscs in at least one stage of their complex life cycle. Trematodes leave characteristic oval-shaped pits with raised rims on the interior of their bivalve hosts, and these pits are preserved in the fossil record. Here we survey 11,785 valves from the Pleistocene–Holocene deposits of the Po Plain and from nearby modern coastal environments on the northeast Adriatic coast of Italy. Of these, 205 valves exhibited trematode-induced pits. Trematodes were selective parasites in terms of host taxonomy and host body size. Infestation was restricted to lower shoreface/transition-to-platform paleoenvironments. During the Holocene, individuals from the transgressive systems tract were significantly more likely to be infested than those from highstand systems tracts. Temporal trends in infestation frequency cannot be explained as an ecological/evolutionary phenomenon (e.g., the hypothesis of escalation); instead the trend seems controlled by environmental variation induced by glacio-eustatic sea-level changes and inadequate sampling. Because this interaction appears to be ephemeral, both temporally and spatially, it is not likely that any selective pressure would be continuous over geologic time in this region. Furthermore, these results support the hypothesis that antagonistic interactions are lower in the northern Adriatic Sea in comparison to other midlatitude shallow marine settings.

Geographic variation of parasitic and predatory traces on mollusks in the northern Adriatic Sea, Italy: implications for the stratigraphic paleobiology of biotic interactions

Abstract. Parasitic trematode worms leave characteristic pits in their bivalve mollusk hosts and represent an ideal system for analyzing parasite-host interactions through space and time with statistically meaningful sample sizes. Previous work in Late Pleistocene—Holocene sequences from the Po plain revealed significant long-term fluctuations in trematode prevalence values: higher prevalence in retrogradational environments (TST) and negligible prevalence in progradational environments (HST). Here we expand upon this work by investigating traces of parasitism, kleptoparasitism, and predation on mollusk death assemblages from two domains along the northern Adriatic coastline. The domain north of the Po delta (TST-like) and the southern domain (including the Po delta; HST-like) comprise environments comparable to those recovered in late Holocene (<6 Kyr) subsurface progradational deposits. We collected 17,299 specimens representing 111 species from 11 locations on the northern Adriatic coast of Italy. Our results reveal high predation pressure, a high diversity of host taxa, and widespread presence of trematode infestation in starved, oligotrophic, environmentally more stable (i.e., TST-like) settings north of the Po delta. Immediately south of the Po delta, in settings with strong and variable sedimentary input, almost no infestation is recorded. The reappearance of infestation is evident in the southern portion of the study area (i.e., Cattolica-Montemarciano), relatively far from the highly stressed environments south of the Po River. There is no significant difference in trematode prevalence values between fossil and modern samples. The distribution of spionid traces (an indicator of stressed environments) was nearly the opposite of that displayed by trematodes. Drilling frequency is highest in TST-like environments and is not correlated with diversity indices. These results suggest that temporal trends of trematode prevalence (and possibly also other biotic interactions) in sedimentary successions are controlled by environmental changes driven by glacio-eustatic dynamics, and reaffirm the importance of interpreting temporal trends in the context of spatial variation.

A complete Holocene record of trematode–bivalve infection and implications for the response of parasitism to climate change

Significance There is growing concern about how parasites will respond to climate change. Previous studies were based on data from short time scales (10−1 to 103 y), but here we present, to our knowledge, the first analysis of the response of parasites to global change on a longer time scale (104 y), utilizing the subfossil record. A 9,600-y record of clams and flatworm parasites from the Pearl River Delta exhibits a significant spike in parasite prevalence during the initial phase of sea-level rise. This increase is not related to changes in salinity or intermediate host availability. Temperature and productivity cannot be quantified and tested as driving factors. These results suggest stark implications for macrobenthos, fisheries, and human health in the context of climate change. Increasing global temperature and sea-level rise have led to concern about expansions in the distribution and prevalence of complex-lifecycle parasites (CLPs). Indeed, numerous environmental variables can influence the infectivity and reproductive output of many pathogens. Digenean trematodes are CLPs with intermediate invertebrate and definitive vertebrate hosts. Global warming and sea level rise may affect these hosts to varying degrees, and the effect of increasing temperature on parasite prevalence has proven to be nonlinear and difficult to predict. Projecting the response of parasites to anthropogenic climate change is vital for human health, and a longer term perspective (104 y) offered by the subfossil record is necessary to complement the experimental and historical approaches of shorter temporal duration (10−1 to 103 y). We demonstrate, using a high-resolution 9,600-y record of trematode parasite traces in bivalve hosts from the Holocene Pearl River Delta, that prevalence was significantly higher during the earliest stages of sea level rise, significantly lower during the maximum transgression, and statistically indistinguishable in the other stages of sea-level rise and delta progradation. This stratigraphic paleobiological pattern represents the only long-term high-resolution record of pathogen response to global change, is consistent with fossil and recent data from other marine basins, and is instructive regarding the future of disease. We predict an increase in trematode prevalence concurrent with anthropogenic warming and marine transgression, with negative implications for estuarine macrobenthos, marine fisheries, and human health.

TOWARDS ESTABLISHING A MODERN BASELINE FOR PALEOPATHOLOGY: TRACE-PRODUCING PARASITES IN A BIVALVE HOST

Abstract One hundred one individuals of Protothaca staminea were live-collected from Argyle Lagoon (sand/mud substrate) and Argyle Creek (gravel/sand substrate), San Juan Island, Washington and examined for trace-producing parasite infestation. Eighty-six percent of individuals contained at least one parasite-induced trace. Trematode-induced pits and blisters were identified on 62% of individual clams. Spionid-induced mudblisters and u-shaped borings were identified on 50% and 29% of individuals, respectively. Trematode and spionid parasites were not selective between the left and right valve when infesting the host. Epifaunal clams from Argyle Creek were significantly smaller than their infaunal counterparts from Argyle Lagoon. This size discrepancy between environments may be related to the reduction of growth rates triggered by environmental stress or parasitism, increased susceptibility to durophagous predators, differences in hydrodynamics, or the comparison of different cohorts. Spionid mudblister-infested clams from Argyle Creek are significantly smaller than noninfested clams from the same environment. This suggests that substrate-induced epifaunality and parasite-induced shell weakening reduced the bivalves’ defenses against durophagous predators. These results suggest that parasites may negatively affect the survival of infested bivalves. The frequent occurrence of trematode and spionid trace-producing parasites in modern bivalve populations suggests that these traces are common in the fossil record, making the systems amenable to study in deep time.

Predation on Modern and Fossil Brachiopods: Assessing Chemical Defenses and Palatability

ABSTRACT The post-Paleozoic decline of the diversity and abundance of rhynchonelliform brachiopods has been attributed to a variety of factors. Of the possible mechanisms invoked to explain the evolutionary decline and cryptic or antitropical distribution of brachiopods, predation has frequently been dismissed due to the potentially low energetic value and suspected nonpalatability or toxicity of brachiopod tissues. Herein we demonstrate that multiple invertebrate marine predators (crustaceans, echinoderms, and gastropods) are willing and able to consume brachiopods in laboratory settings without observable negative effects after ingestion. In addition, field samples indicate predation pressure on the living brachiopod population may be substantial. Although feeding trials are consistent with previous reports that bivalves are preferred prey relative to brachiopods, predation should not be dismissed as a potentially important factor in brachiopod ecology and evolution. The results presented herein reveal that in some cases brachiopods may be the intended target of predatory attacks, especially in habitats where mollusks are rare or absent. Examination of the fossil record of predation on rhynchonelliform brachiopods is consistent with this interpretation: evidence for drilling and repair of brachiopod shells is found throughout the fossil record in multiple lineages. While it is likely that predation traces on post-Paleozoic brachiopods are generally rare, there are multiple reports of fossil localities with anomalously high drill-hole or repair-scar frequencies. This suggests that although brachiopods may be unwanted prey in the presence of energetically more desirable targets, they do appear to be edible and subject to intense predator-prey interactions under certain conditions.

Trace Fossil Evidence of Trematode—Bivalve Parasite—Host Interactions in Deep Time

Parasitism is one of the most pervasive phenomena amongst modern eukaryotic life and yet, relative to other biotic interactions, almost nothing is known about its history in deep time. Digenean trematodes (Platyhelminthes) are complex life cycle parasites, which have practically no body fossil record, but induce the growth of characteristic malformations in the shells of their bivalve hosts. These malformations are readily preserved in the fossil record, but, until recently, have largely been overlooked by students of the fossil record. In this review, we present the various malformations induced by trematodes in bivalves, evaluate their distribution through deep time in the phylogenetic and ecological contexts of their bivalve hosts and explore how various taphonomic processes have likely biased our understanding of trematodes in deep time. Trematodes are known to negatively affect their bivalve hosts in a number of ways including castration, modifying growth rates, causing immobilization and, in some cases, altering host behaviour making the host more susceptible to their own predators. Digeneans are expected to be significant agents of natural selection. To that end, we discuss how bivalves may have adapted to their parasites via heterochrony and suggest a practical methodology for testing such hypotheses in deep time.

Exploratory Multivariate Techniques and Their Utility for Understanding Ancient Ecosystems

Elucidating the ecology and evolution of the early biosphere is a critical area of research in geobiology. Indeed, the number of described species and data sets from early ecosystems has increased rapidly in the last few decades. Such datasets lend themselves well to more complex multivariate analyses. The purpose of this contribution is to serve as a primer for commonly used multivariate ordinations. I review data characterization, as it is critical to selecting the proper ordination. Then I discuss principal components analysis, principal coordinates analysis, non-metric multidimensional scaling, detrended correspondence analysis, and canonical variate analysis. For each ordination I discuss the purpose of the procedure, how it manipulates the data, which types of data are appropriate, and examples of how these procedures have been used to better understand the ecology and evolution of ancient life.