Adiël A. Klompmaker

AN OVERVIEW OF PREDATION EVIDENCE FOUND ON FOSSIL DECAPOD CRUSTACEANS WITH NEW EXAMPLES OF DRILL HOLES ATTRIBUTED TO GASTROPODS AND OCTOPODS

ABSTRACT Predators of extant decapod crustaceans are fairly well known, but unlike many other invertebrate clades, not much is known regarding predation evidence found on fossil decapods. Herein, we provide an overview of such predation and expand upon this through an extensive study of fossil decapod specimens from multiple museum collections. Thus far most examples of predation come from drill holes and stomach contents; bite marks, incisions or irregular holes, and possible regurgitated material are also known. The currently recognized predators of decapods in the fossil record are fish, plesiosaurs, ammonites, octopods, and gastropods. We also provide new evidence of unambiguous drill-hole predation in decapods, based on 33,593 nonmoldic Cenozoic (middle Eocene–Holocene) decapod remains originating from Europe, Asia, and North America, indicating that drilling predation in decapods is more common than currently recognized. Drill holes attributed to octopods (ichnotaxon Oichnus ovalis) and gastropods (O. simplex and O. paraboloides) were found in carapaces and appendages from the Pliocene of the Netherlands, the Pleistocene and Pliocene of the United States (Florida), and the Pleistocene and early Miocene of Japan. Six drill holes attributed to octopods were found in epifaunal and semiburrowing crabs; three drill holes attributed to gastropods were discovered in semiburrowing and epifaunal crabs, and in a burrowing mud shrimp; and the producer of two other drill holes in epifaunal crabs is unknown. Other possible drill holes occur in decapods from the Holocene and early Miocene of Japan and the late Eocene of the United States. Drill-hole predation intensities in decapod faunas by stratigraphic formation are low (≤2.7%), at least in part due to multiple biases such as preservation and molting.

Fossil Crustaceans as Parasites and Hosts.

Numerous crustacean lineages have independently moved into parasitism as a mode of life. In modern marine ecosystems, parasitic crustaceans use representatives from many metazoan phyla as hosts. Crustaceans also serve as hosts to a rich diversity of parasites, including other crustaceans. Here, we show that the fossil record of such parasitic interactions is sparse, with only 11 examples, one dating back to the Cambrian. This may be due to the limited preservation potential and small size of parasites, as well as to problems with ascribing traces to parasitism with certainty, and to a lack of targeted research. Although the confirmed stratigraphic ranges are limited for nearly every example, evidence of parasitism related to crustaceans has become increasingly more complete for isopod-induced swellings in decapods so that quantitative analyses can be carried out. Little attention has yet been paid to the origin of parasitism in deep time, but insight can be generated by integrating data on fossils with molecular studies on modern parasites. In addition, there are other traces left by parasites that could fossilize, but have not yet been recognized in the fossil record.

Revision of Etyidae Guinot and Tavares, 2001 (Crustacea: Brachyura)

Abstract Members of the Etyidae and Feldmanniidae new family have unique arrangements of the spermatheca and gonopores that permit placement of each in different families and that differentiate each from all other brachyurans. Spermathecal openings are not always positioned along the sternal suture between sternites 7 and 8, suggesting that reproductive architecture within the Brachyura and what was formerly regarded as the Podotremata is considerably more diverse and disparate than previously thought. Etyidae and Feldmanniidae radiated in the early Cretaceous and survived into the Paleogene. New taxa include Steorrosia new genus, Bretonia new genus, Faksecarcinus new genus, and sixteen new combinations.

Increase in predator-prey size ratios throughout the Phanerozoic history of marine ecosystems

The size of marine invertebrate predators has increased over the past 500 million years. Bigger and badder The escalation hypothesis posits that predator size has increased over time, leading to increased motility and defense in prey organisms. Although influential, the hypothesis has been difficult to test. Klompmaker et al. looked at predator drill holes in bivalve shells across 500 million years. Drill-hole size did increase, whereas prey size remained relatively constant. This changing predator-prey size ratio suggests that the number of prey consumed likely increased, a factor facilitated by greater complexity of food webs and availability of nutrient-dense prey. Science, this issue p. 1178 The escalation hypothesis posits that predation by increasingly powerful and metabolically active carnivores has been a major driver of metazoan evolution. We test a key tenet of this hypothesis by analyzing predatory drill holes in fossil marine shells, which provide a ~500-million-year record of individual predator-prey interactions. We show that drill-hole size is a robust predictor of body size among modern drilling predators and that drill-hole size (and thus inferred predator size and power) rose substantially from the Ordovician to the Quaternary period, whereas the size of drilled prey remained stable. Together, these trends indicate a directional increase in predator-prey size ratios. We hypothesize that increasing predator-prey size ratios reflect increases in prey abundance, prey nutrient content, and predation among predators.

Growth, inter- and intraspecific variation, palaeobiogeography, taphonomy and systematics of the Cenozoic ghost shrimp Glypturus

Studies in systematic palaeontology are greatly aided when numerous, well-preserved specimens are available so that quantitative methods can be used to substantiate qualitative observations. This is often not the case for fossil decapod crustaceans due to their relatively low preservation potential. Here, we examined primarily two large collections of the well-preserved ghost shrimp Glypturus from the Holo-Pleistocene of Panama and the late Miocene of Florida. Using descriptive, bivariate, multivariate and geometric morphometric methods, two new species are described based on appendage material: Glypturus panamacanalensis sp. nov. and G. sikesi sp. nov. New characters are identified, and size-related and intraspecific variation are assessed for these taxa and modern G. acanthochirus. Taxonomic placement of single specimens from other localities was confirmed by multivariate methods. Furthermore, Glypturus is revised, especially with regard to Western Atlantic species that inhabited both carbonate and siliciclastic environments. Callianassa anguillensis, C. latidigata, and Neocallichirus? quisquellanus are referred to as Glypturus sp. until more material is available to determine the validity of these species. Diversity within Glypturus may thus be underestimated, thereby also impacting the assessment of phylogenetic relationships. Minor propodi appear under-represented relative to major propodi, suggesting a taphonomic bias. Single specimens of interest include a specimen of G. panamacanalensis sp. nov. exhibiting a peculiar swelling in the fixed finger and another showing damage on the propodal upper margin, suggesting failed predation or antagonistic behaviour. Glypturus is first found in the Oligocene in the Western Atlantic and may have expanded its palaeobiogeographical range since the Miocene. The genus was still present on the Pacific side of the Isthmus of Panama in the Holo-Pleistocene, but is only known from the Western Atlantic today, suggesting a relatively recent extinction on the Pacific side. http://zoobank.org/urn:lsid:zoobank.org:pub:C7F0C071-F2AD-4684-B277-037B6F91BF0E

Evolution of body size, vision, and biodiversity of coral-associated organisms: evidence from fossil crustaceans in cold-water coral and tropical coral ecosystems

BackgroundModern cold-water coral and tropical coral environments harbor a highly diverse and ecologically important macrofauna of crustaceans that face elevated extinction risks due to reef decline. The effect of environmental conditions acting on decapod crustaceans comparing these two habitats is poorly understood today and in deep time. Here, we compare the biodiversity, eye socket height as a proxy for eye size, and body size of decapods in fossil cold-water and tropical reefs that formed prior to human disturbance.ResultsWe show that decapod biodiversity is higher in fossil tropical reefs from The Netherlands, Italy, and Spain compared to that of the exceptionally well-preserved Paleocene (Danian) cold-water reef/mound ecosystem from Faxe (Denmark), where decapod diversity is highest in a more heterogeneous, mixed bryozoan-coral habitat instead of in coral and bryozoan-dominated facies. The relatively low diversity at Faxe was not influenced substantially by the preceding Cretaceous/Paleogene extinction event that is not apparent in the standing diversity of decapods in our analyses, or by sampling, preservation, and/or a latitudinal diversity gradient. Instead, the lower availability of food and fewer hiding places for decapods may explain this low diversity. Furthermore, decapods from Faxe are larger than those from tropical waters for half of the comparisons, which may be caused by a lower number of predators, the delayed maturity, and the increased life span of crustaceans in deeper, colder waters. Finally, deep-water specimens of the benthic crab Caloxanthus from Faxe exhibit a larger eye socket size compared to congeneric specimens from tropical reefs, suggesting that dim light conditions favored the evolution of relatively large eyes.ConclusionsThe results suggest a strong habitat control on the biodiversity of crustaceans in coral-associated environments and that the diversity difference between deep, cold-water reefs and tropical reefs evolved at least ~63 million years ago. Futhermore, body size and vision in crustaceans evolved in response to environmental conditions in the deep sea. We highlight the usefulness of ancient reefs to study organismal evolution and ecology.

Trace fossil evidence of coral-inhabiting crabs (Cryptochiridae) and its implications for growth and paleobiogeography

Members of the Cryptochiridae are small, fragile, symbiotic crabs that live in domiciles in modern corals. Despite their worldwide occurrence with over 50 species known today, their fossil record is unknown. We provide the first unambiguous evidence of cryptochirids in the fossil record through their crescentic pits, typical for certain cryptochirids, in Western Atlantic fossil corals, while the Eocene genus Montemagrechirus is excluded from the Cryptochiridae and referred to Montemagrechiridae fam. nov. Nine Pleistocene corals with crescentic pits originate from Florida (USA), and single specimens with pits come from the late Pleistocene of Cuba and the late Pliocene of Florida, all of which are measured for growth analyses. These pits represent trace fossils named Galacticus duerri igen. nov., isp. nov. A study of modern cryptochirid domicile shape (crescentic pit, circular-oval pit, or a true gall) shows that species within crab genera tend to inhabit the same pit shape. Crescentic pits in corals occur not only in the Western Atlantic today, but also in the Indo-West Pacific and in the Eastern Pacific. Thus, examination of Cenozoic fossil coral collections from these regions should yield further examples of cryptochirid pits, which would help to constrain the antiquity of this cryptic crab family.

Possible shell disease in 100 million-year-old crabs.

Modern organisms exhibit evidence of many diseases, but recognizing such evidence in fossils remains difficult, thus hampering the study of the evolution of disease. We report on 2 molts of the goniodromitid crabs Distefania incerta and Goniodromites laevis from the mid-Cretaceous (late Albian) of Spain, with both species exhibiting damage to the dorsal carapace in otherwise well-preserved specimens. The subcircular to quadratical holes, found in <0.2% of the specimens, resemble damage caused by bacterial infections on the cuticle of modern decapods in terms of size and shape. Abiotic damage, predation, and encrustation followed by damage to the shell provide less satisfactory explanations, although these agents cannot be completely excluded from a role in shell disease etiology. We hypothesize that the observed fossil lesions are caused primarily by bacterial disease that started prior to molting, with or without other agents of initiation. If correct, this is the only known example of such bacterial infections in decapod crustaceans from the fossil record thus far, pushing back the evolutionary history of this type of shell disease by ~100 million years.

Extreme rarity of competitive exclusion in modern and fossil marine benthic ecosystems

Competitive interactions have been invoked as major drivers of ecological and evolutionary trends through time, but the strength and frequency of such interactions is notoriously difficult to evaluate. Here we use inferences from species co-occurrence patterns to determine the frequency of the extreme endmember of competition—competitive exclusion—in modern and fossil benthic marine invertebrate assemblages. Within environmentally and temporally well-constrained species pools, we examine the percentage of all species pairs that co-occur less often than expected by chance (segregated pairs) as a maximum measure of competitive exclusion. Segregated pairs are very rare, with most assemblages containing none, and the frequency of segregated pairs shows no trend throughout the Phanerozoic. Contrary to the competition-relatedness hypothesis, we find little evidence that segregated pairs are more common among closely related species except potentially for congeneric pairs in deeper water settings where physical disturbance is relatively low. Although taphonomy, post-mortem transport, and time-averaging could obscure original co-occurrence patterns, analyses suggest that these factors are unlikely to fully explain the low frequency of segregated pairs. Our findings support the hypothesis that predation and disturbance keep marine benthic communities below carrying capacity and thus reduce the potential for competitive interactions to dictate community composition in shallow waters. INTRODUCTION Marine ecosystems have become more taxonomically and ecologically diverse throughout the Phanerozoic (Bambach et al., 2007; Alroy et al., 2008), and several lines of evidence suggest that this diversification may have been facilitated or driven by increasingly complex ecological interactions (Wagner et al., 2006; Huntley and Kowalewski, 2007; Nürnberg and Aberhan, 2015). The rich fossil record of drill holes, scars, and other traces in a variety of invertebrates provides some evidence that predation and parasitism have become more common through time (Huntley and Kowalewski, 2007; Klompmaker and Boxshall, 2015), but quantifying evidence of competition has been more difficult. With the exception of overgrowth relationships in encrusting taxa (Taylor, 2016), direct evidence of interspecific competition is extremely rare. Hence, the role of competition in marine ecosystems through time remains poorly understood. Although competition is a cornerstone of evolutionary theory (Darwin, 1859) and has been invoked to explain some major clade replacements (Stanley and Newman, 1980; Sepkoski et al., 2000; Liow et al., 2015), others have argued that competition is not a major evolutionary force in marine ecosystems (Benton, 1996; Stanley, 2008; Myers and Lieberman, 2011). It is difficult to quantify the strength of competitive interactions among modern marine species and impossible to do so for most fossil species, but it may be possible to recognize competitive exclusion, the extreme endmember of competition in which two species with identical niches cannot locally coexist (Hardin, 1960). Here we employ a recently developed analytical approach (Lyons et al., 2016, and references therein) to evaluate the frequency of competitive exclusion in fossil and modern benthic marine invertebrate assemblages. We examine cooccurrence patterns within local species pools to determine whether species pairs co-occur less often than expected by chance (segregated or negative pairs) (Sfenthourakis et al., 2006). We assess (1) the commonness of competitive exclusion, as measured by the percentage of segregated species pairs of all pairs within assemblages, in modern and fossil marine assemblages through time; (2) whether segregated pairs occur more often among closely related taxa, as predicted by the competition-relatedness hypothesis (Cahill et al., 2008) originally proposed by Charles Darwin (Darwin, 1859); and (3) whether the frequency and taxonomic distribution of segregated pairs is affected by water depth, a rough proxy for disturbance frequency and strength.