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Some characteristics of Aspergillus and Penicillium make them particularly likely to

cause infections and mortality of avian eggs. Aspergillus (Oglesbee, 1997) and

Penicillium (Pitt, 1979) are extremely diverse and widespread genera found in soil, leaf litter and in the air, and although not every species within each genus is pathogenic, they are both characterised as having high pathological importance. Both groups contain many toxic species and many capable of causing cell destruction (Hubalek et al., 1973; Baker and Bennett, 2008; Geiser, 2009). Several characteristics of Aspergillus

and Penicillium increase the likelihood of them impacting NIBK hatching success.

The morphology and growth of Aspergillus and Penicillium facilitates their penetration into the eggshell. The hyphal growth of both genera has been shown to have the potential to break through the protective egg cuticle and open the pores up to bacterial invasion (Board and Fuller, 1974). The conidia (asexually produced spores) of both genera are more than small enough to penetrate the pores of eggshells. For example, the conidia of Aspergillus spp. average 3-3.9 μm diameter (Hess and Stocks, 1969) and the conidia of Penicillium spp. 2-4 μm (Pitt, 1979), while the pores of NIBK eggs range from 10-100 μm (Silyn-Roberts, 1983).

Thermophily (the ability to persist at high temperatures) is another characteristic of some members within both fungal genera. This trait allows these fungi to persist at conditions outside the range of most fungi, with the optimal temperature for some

species being the same temperature as incubated eggs, 35-37oC. Some Penicillium

species can survive at temperatures as low as 5oC (Carlile et al., 2001), which means survival when the egg is un-incubated. Aspergillus and Penicillium species can tolerate,

grow and even thrive in dry and low nutrient conditions, and have the ability to enter dormancy in certain life stages (Carlile et al., 2001). Both these traits influence their virulence and facilitate their roles as a pathogen because they increase their ability to survive on the dry, potentially low nutrient eggshell.

Members of the Aspergillus genera have also been shown to have the ability to

chelate, transport and store iron (Krappmann, 2008). This is a prerequisite for microbial pathogens as iron is essential for rapid growth (Haas, 2003). This trait could facilitate growth in the egg, as iron is limited within the albumen due to proteins such as ovotransferrin which chelate iron (Kobayashi et al., 1996; Krappmann, 2008).

Finally, there are the toxic secondary metabolites produced by both fungi groups, which increase their potential to negatively impact NIBK hatching success. Some of these toxins have been shown to cause death in young and adult birds but have also been shown to severely impact growth, development and survival of avian embryos (Scott, 1977; Todd and Bloom, 1980; Potchinsky and Bloom, 1993; Qureshi et al., 1998).

There are over 400 known secondary metabolites produced by Aspergillus species with over 70 of these being known toxins (mycotoxins) (Bartholomew, 2013). For example:

aflatoxin, produced by some species of Aspergillus, is one of the most potent

carcinogens known to man (Abundis-Santamaria, 2003). In the domestic chicken, exposure to aflatoxin has been shown to cause DNA damage in developing embryos, lead to reduced fertility, reduced hatchability of fertile eggs and increased embryo death (Todd and Bloom, 1980; Potchinsky and Bloom, 1993; Qureshi et al., 1998) . The

Penicillium genus is also noted for the diverse array of mycotoxins produced by some species. Citreoviridin for example has been shown to lead to rapid death in a range of birds due to damage to the central nervous system (Scott, 1977); whilst penicillic acid has been shown to cause embryo death and also cell necrosis in several animal species (Ciegler et al., 1972; Scott, 1977). Some serious mycotoxins are produced by both

Aspergillus and Penicillium species; for example, both genera produce citrinin and ochratoxin, which in turn cause serious health impacts to embryos and adult birds. Ochratoxin can cause liver and kidney damage in a range of animals and has also been

shown to be severely teratogenic (causes embryo malformations) in birds (Edrington et al., 1995). Ochratoxin causes rapid and excessive embryo cell death in chickens and has been linked with serious malformations in areas such as the spinal cord and hindgut (Wei and Sulik, 1996). Citrinin has been shown to cause kidney failure in chickens and can lead to embryo death (Flajs and Peraica, 2009).

Not all secondary metabolites have negative effects; the antimicrobial action of some of the secondary metabolites may in fact provide a benefit as they can restrict the growth of other, more pathogenic microbes that could increase egg health over the incubation period. Both groups also possess harmless species, which may have no impact on the egg or developing embryo. Benefits to the avian embryo, through mechanisms such as competitive exclusion, have been shown for bacteria (McCabe, 1967) (see chapter three), but no such work has been done on potential benefits of fungi. Fumagillin is a secondary metabolite produced by some Aspergillus spp. that is bothanantibiotic and an antiprotozoal agent (Eble and Hanson, 1951). There are also

secondary compounds produced by the Penicillium genera that have been shown to

have anti-viral and anti-bacterial properties such as statolon (Kleinschmidt and Murphy, 1965; Pitt, 1979) and penicillin (Garrod, 1960). Although the fungi may exclude bacteria through the production of such antimicrobials, the hyphal growth could still compromise the shell structure and lead to a negative impact. The positive impact of fungi on avian eggshells is an area open to more research. However, the pathogenic characteristics of both Aspergillus and Penicillium species make them a threat to the hatching success of kiwi and further studies are needed to determine their impact.