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

BACKGROUND: Modern 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. RESULTS: We 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. CONCLUSIONS: The 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.

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.

Environmental and scale-dependent evolutionary trends in the body size of crustaceans.

The ecological and physiological significance of body size is well recognized. However, key macroevolutionary questions regarding the dependency of body size trends on the taxonomic scale of analysis and the role of environment in controlling long-term evolution of body size are largely unknown. Here, we evaluate these issues for decapod crustaceans, a group that diversified in the Mesozoic. A compilation of body size data for 792 brachyuran crab and lobster species reveals that their maximum, mean and median body size increased, but no increase in minimum size was observed. This increase is not expressed within lineages, but is rather a product of the appearance and/or diversification of new clades of larger, primarily burrowing to shelter-seeking decapods. This argues against directional selective pressures within lineages. Rather, the trend is a macroevolutionary consequence of species sorting: preferential origination of new decapod clades with intrinsically larger body sizes. Furthermore, body size evolution appears to have been habitat-controlled. In the Cretaceous, reef-associated crabs became markedly smaller than those in other habitats, a pattern that persists today. The long-term increase in body size of crabs and lobsters, coupled with their increased diversity and abundance, suggests that their ecological impact may have increased over evolutionary time.

Exploring the preservation of a parasitic trace in decapod crustaceans using finite elements analysis.

The fossil record of parasitism is poorly understood, due largely to the scarcity of strong fossil evidence of parasites. Understanding the preservation potential for fossil parasitic evidence is critical to contextualizing the fossil record of parasitism. Here, we present the first use of X-ray computed tomography (CT) scanning and finite elements analysis (FEA) to analyze the impact of a parasite-induced fossil trace on host preservation. Four fossil and three modern decapod crustacean specimens with branchial swellings attributed to an epicaridean isopod parasite were CT scanned and examined with FEA to assess differences in the magnitude and distribution of stress between normal and swollen branchial chambers. The results of the FEA show highly localized stress peaks in reaction to point forces, with higher peak stress on the swollen branchial chamber for nearly all specimens and different forces applied, suggesting a possible shape-related decrease in the preservation potential of these parasitic swellings. Broader application of these methods as well as advances in the application of 3D data analysis in paleontology are critical to understanding the fossil record of parasitism and other poorly represented fossil groups.

Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.

Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

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

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.

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.

Systematics, phylogeny, and taphonomy of ghost shrimps (Decapoda): a perspective from the fossil record.

Ghost shrimps of Callianassidae and Ctenochelidae are soft-bodied, usually heterochelous decapods representing major bioturbators of muddy and sandy (sub)marine substrates. Ghost shrimps have a robust fossil record spanning from the Early Cretaceous (~ 133 Ma) to the Holocene and their remains are present in most assemblages of Cenozoic decapod crustaceans. Their taxonomic interpretation is in flux, mainly because the generic assignment is hindered by their insufficient preservation and disagreement in the biological classification. Furthermore, numerous taxa are incorrectly classified within the catch-all taxon Callianassa. To show the historical patterns in describing fossil ghost shrimps and to evaluate taphonomic aspects influencing the attribution of ghost shrimp remains to higher level taxa, a database of all fossil species treated at some time as belonging to the group has been compiled: 250 / 274 species are considered valid ghost shrimp taxa herein. More than half of these taxa (160 species, 58.4%) are known only from distal cheliped elements, i.e., dactylus and / or propodus, due to the more calcified cuticle locally. Rarely, ghost shrimps are preserved in situ in burrows or in direct association with them, and several previously unpublished occurrences are reported herein. For generic assignment, fossil material should be compared to living species because many of them have modern relatives. Heterochely, intraspecific variation, ontogenetic changes and sexual dimorphism are all factors that have to be taken into account when working with fossil ghost shrimps. Distal elements are usually more variable than proximal ones. Preliminary results suggest that the ghost shrimp clade emerged not before the Hauterivian (~ 133 Ma). The divergence of Ctenochelidae and Paracalliacinae is estimated to occur within the interval of Hauterivian to Albian (133-100 Ma). Callichirinae and Eucalliacinae likely diverged later during the Late Cretaceous (100-66 Ma), whereas Callianassinae did not appear before the Eocene (56 Ma).

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.

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.

Spider crabs of the Western Atlantic with special reference to fossil and some modern Mithracidae.

Spider crabs (Majoidea) are well-known from modern oceans and are also common in the western part of the Atlantic Ocean. When spider crabs appeared in the Western Atlantic in deep time, and when they became diverse, hinges on their fossil record. By reviewing their fossil record, we show that (1) spider crabs first appeared in the Western Atlantic in the Late Cretaceous, (2) they became common since the Miocene, and (3) most species and genera are found in the Caribbean region from the Miocene onwards. Furthermore, taxonomic work on some modern and fossil Mithracidae, a family that might have originated in the Western Atlantic, was conducted. Specifically, Maguimithrax gen. nov. is erected to accommodate the extant species Damithrax spinosissimus, while Damithrax cf. pleuracanthus is recognized for the first time from the fossil record (late Pliocene-early Pleistocene, Florida, USA). Furthermore, two new species are described from the lower Miocene coral-associated limestones of Jamaica (Mithrax arawakum sp. nov. and Nemausa windsorae sp. nov.). Spurred by a recent revision of the subfamily, two known species from the same deposits are refigured and transferred to new genera: Mithrax donovani to Nemausa, and Mithrax unguis to Damithrax. The diverse assemblage of decapods from these coral-associated limestones underlines the importance of reefs for the abundance and diversity of decapods in deep time. Finally, we quantitatively show that these crabs possess allometric growth in that length/width ratios drop as specimens grow, a factor that is not always taken into account while describing and comparing among taxa.

Parasites in the fossil record: a Cretaceous fauna with isopod-infested decapod crustaceans, infestation patterns through time, and a new ichnotaxon.

Parasites are common in modern ecosystems and are also known from the fossil record. One of the best preserved and easily recognisable examples of parasitism in the fossil record concerns isopod-induced swellings in the branchial chamber of marine decapod crustaceans. However, very limited quantitative data on the variability of infestation percentages at the species, genus, and family levels are available. Here we provide this type of data for a mid-Cretaceous (upper Lower Cretaceous, upper Albian) reef setting at Koskobilo, northern Spain, on the basis of 874 specimens of anomurans and brachyurans. Thirty-seven specimens (4.2%), arranged in ten species, are infested. Anomurans are more heavily infested than brachyurans, variability can be high within genera, and a relationship may exist between the number of specimens and infestation percentage per taxon, possibly suggesting host-specificity. We have also investigated quantitative patterns of infestation through geological time based on 88 infested species (25 anomurans, 55 brachyurans, seven lobsters, and one shrimp), to show that the highest number of infested species can be found in the Late Jurassic, also when corrected for the unequal duration of epochs. The same Late Jurassic peak is observed for the percentage of infested decapod species per epoch. This acme is caused entirely by infested anomurans and brachyurans. Biases (taphonomic and otherwise) and causes of variability with regard to the Koskobilo assemblage and infestation patterns through time are discussed. Finally, a new ichnogenus and -species, Kanthyloma crusta, are erected to accommodate such swellings or embedment structures (bioclaustrations).

Animal behavior frozen in time: gregarious behavior of Early Jurassic lobsters within an ammonoid body chamber.

Direct animal behavior can be inferred from the fossil record only in exceptional circumstances. The exceptional mode of preservation of ammonoid shells in the Posidonia Shale (Lower Jurassic, lower Toarcian) of Dotternhausen in southern Germany, with only the organic periostracum preserved, provides an excellent opportunity to observe the contents of the ammonoid body chamber because this periostracum is translucent. Here, we report upon three delicate lobsters preserved within a compressed ammonoid specimen of Harpoceras falciferum. We attempt to explain this gregarious behavior. The three lobsters were studied using standard microscopy under low angle light. The lobsters belong to the extinct family of the Eryonidae; further identification was not possible. The organic material of the three small lobsters is preserved more than halfway into the ammonoid body chamber. The lobsters are closely spaced and are positioned with their tails oriented toward each other. The specimens are interpreted to represent corpses rather than molts. The lobsters probably sought shelter in preparation for molting or against predators such as fish that were present in Dotternhausen. Alternatively, the soft tissue of the ammonoid may have been a source of food that attracted the lobsters, or it may have served as a long-term residency for the lobsters (inquilinism). The lobsters represent the oldest known example of gregariousness amongst lobsters and decapods in the fossil record. Gregarious behavior in lobsters, also known for extant lobsters, thus developed earlier in earth's history than previously known. Moreover, this is one of the oldest known examples of decapod crustaceans preserved within cephalopod shells.