A newly recognized Mesozoic–Recent interspecific association: calcifying bacteria on decapod crustaceans

Abstract

Using microscopy and spectroscopy tools, we succeeded in identifying undescribed diminutive epibionts (as epibiotic bacterial colonies) both on exceptionally well‐preserved fossil shrimps and on extant taxa (N. Robin, S. Bernard, J. Miot, M.‐M. Blanc‐Valleron, S. Charbonnier & G. Petit, submitted). This study outlines the ecological parameters of this totally newly recognized interspecific association. To this aim, the systematics and environmental setting of fossil and modern decapod hosts are described; count of bacterial colonies is made to assess prevalence and intensity; scanning electron microscopy is used to illustrate colonial growth patterns; and histological sections of the extant colonies nested in cuticle are stained to determine their incidence on the carapace of their decapod hosts. Thus, the prevalent and intense association is found on decapods of the superfamily Penaeoidea Rafinesque‐Schmaltz 1815 occupying up to 2 cm2 of the entire carapace. The association is here observed in deep environments such as that of the Jurassic La Voulte‐sur‐Rhône Lagerstätte. A non‐random distribution of colonial growth patterns is determined; it illustrates a favourite access site along the ventral margin of the shrimp carapace. SEM images and stained sections reveal strong colony embedment within the cuticle, but also damage such as erasing of the cuticular layers. This bioeroding effect, possibly linked to a feeding benefit to the bacteria, brings this interspecific association that has existed, for at least 160 myr, near to parasitism. In addition to illustrating a rare case of interaction in Recent forms that could be described due to previous recognition in fossils, it constitutes a textbook example of the preservation of intimate interactions through geological time.

Decapod crustaceans from the Paleocene (Danian) of the Paris Basin (Vigny stratotype and allied localities) and a limpet palaeoassociation

“…This interspecific association is too short to involve any phenotypical pressures on the temporary partners, unlike in commensalism or parasitism that involve long-lasting associations (e.g. Weinberg- Rasmussen et al 2008;Klompmaker et al 2014, for isopod-induced swellings in the branchial region of decapods; Robin et al 2015, for epicuticle erosion by colonial bacteria).…”

Calcification and Diagenesis of Bacterial Colonies

“…As the investigated contemporary and fossilized epibiotic structures share numerous similarities down to the submicrometer scale, the fossilized epibiotic structures are interpreted as fossilized calcifying epibiotic bacterial colonies. Of note, a palaeoecological complementary study has revealed the probable ectoparasitic habit of these bacterial colonies [11]. This symbiosis close to parasitism has thus existed for at least 160 myr.…”

“…These shrimps and their epibiotic bacterial colonies have been caught alive in the La Paz Bay (Mexico) and preserved, since their capture, in 70% alcohol in order to maintain their structural and chemical integrity. Epibiotic organo-mineral structures have been detected on the whole carapace (pleon, carapace and telson) of most of the 20 sampled specimens, covering up to 10% of the whole animal ( Figure 1) [11].…”

“…Epibiosis, the association between two species in which one (the epibiont) spends a portion of its life attached to the surface of the second one (the basibiont) [1], has likely involved a broad diversity of taxa over geological time as evidenced by a number of studies having reported fossilized symbiotic organisms [2][3][4][5][6][7][8][9][10][11][12]. Yet, identifying such ancient interspecific associations in the fossil record may be challenging in the case of epibiotic micro-organisms, notably because of their poor resistance to diagenetic degradation.…”

The first record of paguroids from the Eocene of Istria (Croatia) and further phylogenetic refinement of the Paguroidea (Crustacea, Anomura)

“…However, the flattening of the tubercles appear to correspond to hindrance during the production of superficial cuticular layers (as already postulated in the case of ectosymbiotic bacterial colonies; see Robin et al 2015) rather than to true abrasion of the tubercles that could have occurred as a result of post-mortem epibiont attachment. This would hardly be observed in a post-mortem association, but would more reliably be the result of a syn-vivo association with the anomuran.…”