Fungi in a Lower Cretaceous Turtle Egg From China: Evidence of Ecological Interactions

Abstract

Fossil fungi and arthropod body parts are present in one of 27 unhatched eggs in a turtle egg clutch from the Lower Cretaceous (Albian) Liangtoutang Formation, Zhejiang Province, China. The fossil fungal structures include branching septate hyphae, conidiophores supporting multiple phialides, and chains of up to five basipetal conidia (asexual spores). The morphology of the fossil fungus is similar to extant taxa within the genus Penicillium (order Eurotiales), making it the first reported intact Early Cretaceous asexual ascomycete and the earliest record of a presumed intact Penicillium. Biomineralization, a physiologic response to calcium-rich microenvironments, occurs in some extant fungi and may have facilitated detailed preservation of the fossil specimen. This rare evidence of fungal-animal association provides clues to clutch-related paleoecological interactions. The fungus-bearing egg occurs on the clutch periphery, whereas adjacent and more distant eggs show no evidence of fungal invasion. We suggest that the fungi were opportunistic contaminants invading after the egg was compromised, and the fungus failed to spread to adjacent eggs prior to burial and fossilization.

A Review of the Fossil Record of Turtle Reproduction: Eggs, Embryos, Nests and Copulating Pairs

“…The thick, rigid eggshell and spherical egg shape likely reduced the possibility of lethal desiccation because the greater pore length and reduced surface area retarded water loss during incubation. In addition, the specimen reveals rare evidence of fungal-animal association in the fossil record (Jackson et al 2009). A single egg on the periphery of the clutch contains fossil fungal structures, suggesting opportunistic fungal invasion after the egg was compromised and prior to subsequent failure of the clutch as a whole.…”

“…[11] Early Cretaceous, Albian and Late Cretaceous, Cenomanian-Turonian; Liangtoutang and Chichengshan formations, respectively; Zhejiang Province; Testudoolithus jiangi; egg and clutch (Fang et al 2003;Jin 2009) Bulletin of the Peabody Museum of Natural History 55(2) • October 2014…”

Fungal Ferromanganese Mineralisation in Cretaceous Dinosaur Bones from the Gobi Desert, Mongolia

“…[ 3 , 65 ]); as a result mineral phases such as birnessite, ferrihydrite, goethite, hematite, todorokite, halloysite, and montmorillonite often crystallise around thalli ([ 3 ] and reference therein). These inlays and auto mineralisation can survive in the fossil record, as in the case of fungal hyphae and conidia found in fossilised eggs of turtles from the Chinese Liangtoutang Formation [ 23 ]. Santelli et al [ 66 ] noted that Mn-oxidising bacteria are the main focus of recent studies, although in many terrestrial environments fungal Mn and Fe oxidation may also be important ([ 66 ] and reference therein; [ 65 ]).…”

“…Ascomycete fungi such as Acremonium [ 66 ] can produce a variety of iron and manganese phases depending on the pH of the surrounding medium and availability of metal ions. Ascomycete fungi are known from the fossil record mostly from amber findings [ 15 , 16 , 17 ] and were found as iron-oxide-mineralised hyphae and conidia from an Early Cretaceous turtle egg clutch [ 23 ].…”

“…The aim of this work is to present the first known case of mineralised fungal or saprolegnia-like mycelia preserved in dinosaur bones exemplified in samples from the Cretaceous Nemegt Formation (Gobi Desert, Mongolia). Following fungal remnants of coprolites from the Lameta Formation (India) [ 22 ] and a Penicillium -like fungus from Early Cretaceous turtle eggs described from the Langtoutang Formation (China) [ 23 ], this is the third example of fossil mycelia associated with vertebrate fossils from Mesozoic strata, and the first finding in the archaeological record of fungal borings and hyphae occuring together in fossil bones. The mycelia described here are the oldest fossil fungal- or saprolegnia-like remains identified from bones to date.…”