Fungianimal Interactions

Despite the obvious role fungi play in modern ecosystems as decomposers, parasites, and mutualists, the interactions between fungi and animals are not extensively documented in the fossil record. A common fungus-animal interaction known from the Paleozoic to the recent is evidence of borings made by endolithic fungi (also algae and bacteria) in calcium carbonate skeletons of marine invertebrates (Gatrall and Golubic, 1970; Grahn, 1981). This represents a trace fossil (or ichnofossil), in that no organic material of the fungus remains, only trace evidence in the form of damage to shells, and so on. Another early example of fungus-animal interactions involves middle Silurian fungal remains from Sweden (Sherwood-Pike and Gray, 1985). These rocks contain spindle-shaped aggregates of hyphae associated with amorphous material up to 260 ^m long. The fungal remains are interpreted as frass (fecal pellets) produced by a micro-arthropod. Another explanation is that the arthropod was using the fecal remains as their primary food source. This example demonstrates the difficulty in determining nutritional modes and interactions in paleoecosystems.

In some cases, the morphological similarity between a fossil and extant fungus can be used to infer the nutritional mode and degree of interaction. Geotrichites glaesarius represents a conidial fungus, that is, a fungus that forms external, asexual spores of a particular type (Stubblefield et al., 1985b). It was found on the surface of a partially decomposed abdomen of a spider (FIG. 3.97 ) preserved in late Oligocene-early Miocene amber from the Dominican Republic (Stubblefield et al., 1985b). The fact that the fungus had not invaded the body cavity of the spider and the pattern of conidial formation suggest that this interaction was saprotrophic. Two other reports of entomophthoralean (Zygomycota) fungi from the Dominican amber include a parasitic infection of a winged termite and a fungus, found on a fossil ant, which resembles modern members of an insect pathogen (Poinar and Thomas,

1982, 1984). From Cenozoic amber collected in Mexico, fungi have even been described inside fossil nematodes (FIG. 3.98) (Poinar, 1984; Jansson and Poinar, 1986). Schmidt et al. (2007; 2008) have reported carnivorous fungi preserved in Cretaceous amber that possess hyphal rings

Nematode Fossil Amber
FIGURE 3.97 Chains of conidia attached to a spider leg preserved in Dominican amber (Miocene). Bar = 50 |im.
FIGURE 3.98 Nematode containing fungus Bar = 15 |im. (From Jansson and Poinar, 1986.)


that serve to trap nematodes (FIGS. 3.99-3.101). Associated with the fungi are small nematodes that probably represented the prey. Modern carnivorous fungi are found in the Zygomycota, Ascomycota, and Basidiomycota, and the presence of these forms in amber indicates that complex devices to trap motile organisms had evolved by the early Cretaceous. Although these reports are important in documenting cases of specific interactions in the fossil record, there are still too few reports currently available from older rocks to make any substantive comment regarding the evolution of these complex interactions.

The associations between fungi and animals are perhaps nowhere more unusual than those known from the

Freshwater Obligate Plant Pictures
FIGURE 3.99 Carnivorous fungus, trapping ring (Cretaceous). Bar = 10 pm. (Courtesy A. Schmidt.)
Cretaceous Fungi
FIGURE 3.100 Carnivorous fungus, yeast-like growth forming along a hypha (Cretaceous). Bar = 10 pm. (Courtesy A. Schmidt.)

Trichomycetes. Today, trichomycetes inhabit the lower digestive tracts of various types of insects and other arthropods, and based on molecular sequences, it is suggested that many groups are polyphyletic (White, 2006). These endosymbiotic microfungi live in freshwater and include more than 130 species; however, this probably represents a fraction of the total number of living forms. In this obligate mutualistic association, the fungi are not capable of existing outside the host gut. The only fossil trichomycete known to date is a specimen from the Triassic of Antarctica (White and Taylor, 1989b) . It consists of a small fragment of presumed arthropod cuticle to which are attached numerous, elongate thalli (FIG. 3.102), each anchored by a holdfast cell. At the distal end of each

Nematode Trapping Fungi
FIGURE 3.101 Reconstruction of the carnivorous (nematode trapping) fungus (Cretaceous). (From Schmidt et al., 2007.)
Nematode Trapping Fungi
FIGURE 3.102 Palisade organization of thalli on the inner surface of putative arthropod cuticle (Triassic). Bar = 100 pm.

thallus is a small plug and numerous spores. Although the diagnostic features of the cuticle necessary to identify the host are not present, the occurrence of numerous fecal pellets associated with plant tissues from the same site substantiates the existence of arthropods in this Triassic ecosystem (Kellogg and E. Taylor, 2004).

Fungal remains have also been documented in a variety of coprolites (FIG. 3.103) and have been especially useful in Quaternary palynology (Davis, 2006 and references therein). In some examples the producers of the coprolites are believed to have been saprobes dwelling on all sorts of organic particles, whereas in other instances a high percentage of the coprolites contain fungal remains, suggesting that the producers were true fungivores (Pratt et al., 1978). Fungi have been reported in various types of dinosaur coprolites, and the presence of certain types of leaf-borne fungi has been used to infer a foliage diet for these animals (Sharma et al., 2005). An interesting report of partially decayed wood found in coprolites of herbivorous dinosaurs (Chin, 2007) suggested that the animals may have eaten wood that had been partially rotted by fungi when there were few other food sources available. The wood would only be useful as a nutrient source after fungi had begun to break down the lignin and cellulose within it. The report and description of fungi associated in other biotic interactions (e.g., additional types of coprolites and a variety of different types of borings) in Miocene wood is an important contribution that will help to underscore the geological history of fungal-animal interactions (Sutherland, 2003).

An unusual interaction between fungi and animals has been documented from the Jurassic (Martill, 1989). On the surface of fossil fish teeth are a series of meandering

Jurassic Flora Brora Sutherland
FIGURE 3.103 Coprolite composed of hyphae (Devonian). Bar = 50 pm.

borings that are restricted to the surface enamel. These have been given the name Mycelites enameloides. Similar borings have been reported on teeth, scales, and bone as early as the Devonian (Gouget and Locquin, 1979). The report of fungal-animal interactions and associations in the fossil record is a very important area in paleomycology. Although many of the associations may be the activities of fungal saprotrophs, others may represent early stages of symbiotic interrelationships that are widespread in modern ecosystems, and which represent one of the cornerstones of biodiversity today (Zook, 2002).

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