Neozygites floridana is a fungus that is an obligate pathogen of spider mites. This species was first discovered in Florida on the Texas citrus mite by Weiser and Muma in 1966. Based on morphology and ecology this fungus is currently classified in subphylum Entomophthoromycotina, order Neozygitales and Family Neozygitaceae. However, the few DNA sequences available for the genus Neozygites suggest that this group is very unique. In a molecular study by White et al. (2006) the genus Neozygites was highly divergent and was not resolved in a clade with other fungi in Entomophthoromycotina. Further studies are needed to resolve the phylogenetic affiliations of this unusual entomophthoralean fungus.
Since its circumscription in 1966, N. floridana has been reported on several other mite hosts and one species of thrips including Mononychellus tanajoa Bondar, Scirtothrips dorsalis Hood, Tetranychus evansi Baker & Pritchard, and Tetranychus urticae Koch across a large geographic distribution (Hountondji et al. 2002;Mikunthan and Manjunatha 2006;Ribeiro et al. 2009). In Brazil, the highest infection rates of N. floridana (syn. T. floridana) occurred from April to June, correlating to a time period following a rainy season (Humber et al. 1981). Neozygites floridana has been associated with epizootic events where spider mite mortality occurs in a large percentage of the active populations (Carner 1976;Duarte et al. 2009;Hountondji et al. 2002;Humber et al. 1981). Generally host population density is critical for epizootic events to occur, and while this holds true for N. floridana, low densities (< 10 mites/3.14cm2) of tomato red spider mite, T. evansi, still yielded high infection incidence of 50% of the population in a controlled experiment (Duarte et al. 2009;Duarte 2013).Globally, where N. floridana is found it is generally associated with a significant reduction of spider mite populations (Carner 1976;Oduor et al. 1996).
Often certain phenotypic or physiological characteristics can predispose organisms to being more prone to infections. Due to cuticular, immunological and behavioral mechanisms, immature and female two-spotted spider mites, T. urticae, were shown to be more susceptible to infections of N. floridana compared to male and mature mites (Susilo et al. 1994).
Biological control is a common practice in integrated pest management (IPM) programs that uses natural enemies or pathogens of pests to reduce populations of pests below an economic threshold so yield is not affected without relying solely on pesticides. Neozygites floridana has been shown to reduce populations of mites and thrips during natural infections especially when host densities are high (Duarte 2013;Mikunthan and Manjunatha 2006). For example, Smith and Furr observed an 82% infection incidence in T. urticae populations in a cotton crop planted in Mississippi (Smith and Furr 1975). In order to incorporate biological control, such as the application of N. floridana, the biological control agent should be compatible with pesticides routinely used on crops, such as fungicides and insecticides. Weseka et al. showed that certain, widely-used fungicides and insecticdes negatively affected the normal life cycle of N. floridana, which could have negative consequences in a realistic IPM program (Wekesa et al. 2008).
Although pesticides negatively impacted N. floridana, Weseka et al. showed that N. floridana was unable to infect the predaceous mite, Phytoseiulus longipes Evans, which is another biological control agent of the two-spotted spider mite, T. urticae (Wekesa et al. 2007). Furthermore, they showed that there was no significant difference in exploration time for P. longipes to search for eggs on leaves with or without capilliconidia. Lastly, there was no preference by P. longipes when given the choice to feed on spider mite eggs on leaf discs with or without capilliconidia (Wekesa et al. 2007). This host specificity is a desirable characteristic when choosing a candidate biological control agent (Duarte 2013).
Although not always observed during epizootic events, resting spores, zygospores or azygospores, are another characteristic that make N. floridana a suitable candidate for biological control (Duarte 2013). These spores serve as a resilient propagule that can survive extremely unsuitable conditions, which could be used to inoculate crops infested with mite pests. Overall, N. floridana, has several characteristics that make it a suitable candidate for use as a biological control agent, and that growers designing integrated pest management systems should be mindful of natural infections, so that pesticide applications are economically and biologically beneficial.
Capilliconidia are the primary infectious propagule of N. floridana, which is due to the adhesive apex of the spore borne on a long capillary tube making more efficient transfer of propagules to hosts (Oduor et al. 1996). In addition these conidia quickly germinate under a wide range of climatic conditions. For example, on the cassava green mite, Mononychellus tanajoa, N. floridana capilliconidia began germinating two hours post attachment to the host at temperatures between 18 and 28°C, and increased humidity resulted in higher germination rates (Oduor et al. 1996).After cappiliconidia attach to host and germinate, the germ tube penetrates the host cuticle and hyphal bodies are produced and multiply by binary fission throughout the host tissues (Keller 1997). During epizootic periods, the asexual life cycle is the primary stage and zygospores, if observed, are only observed late in the season, but this is rare in warmer climates (Carner 1976;Duarte 2013;Oduor et al. 1996). During the asexual stage hyphal bodies will produce conidiophores that erupt through host cuticle tissues and bear primary conidia (Keller 1997). Primary conidia can germinate to form secondary conidia, where both primary and secondary conidia can germinate to form capilliconidia (Carner 1976;Duarte et al. 2009;Keller 1997). Sexual reproduction occurs when two hyphal bodies of different mating types fuse to form a zygospore, which is an overwintering and sexual stage of this fungus (Keller 1997). Azygospore production in Tetranychus urticae was observed in isolates of N. floridana from Brazil as well as Norway (Westrum et al. 2014). This was the result of an overwintering spore being formed from a single hyphal body inside the body of the host tissue (Westrum et al. 2014).
Neozygites floridana produces short, mostly non-branching clavate hyphal bodies that can be found throughout all tissues of an infected host (Weiser and Muma 1966). Single conidiophores (30-35 x 6-8μm) bearing primary conidia erupt through host cuticle tissues from rhizoid-like hyphae (Weiser and Muma 1966). Primary conidia (12 (11-13) x 15 (13-18) μm) are pyriform, axially symmetric, papillate to apapillate with unitunicate, smooth, slightly dark cell walls (Remaudière and Keller 1980;Weiser and Muma 1966). Each primary conidia generally contains four nuclei and are discharged short distances (Remaudière and Keller 1980). Columnellae are persistent and remain intact after spore discharge (Weiser and Muma 1966).
Secondary conidia are produced from a hyphal bud of a primary conidium, and are generally the same size and shape as primary conidia (Weiser and Muma 1966). Anadhesive spores, or capilliconidia, are produced at the ends of slender capillary tubes (1.5 x 50-60μm) produced by primary and secondary conidia (Keller 1997;Weiser and Muma 1966). These spores have a striated, pigmented cuticle and an adhesive apex, which help these spores attach to host arthropods effectively dispersing the spores (Weiser and Muma 1966). The production of capilliconidia are unique to Neozygites and some Condiobolus species separating it from other related “entomophoroid” fungi (Weiser and Muma 1966). In addition, N. floridana does not produce microconidia, which distinguishes it from most Conidiobolus species (Weiser and Muma 1966).
Resting spores are 20-23.5 x 22-26μm in diameter and either sexually produced as zygospores or asexually produced as azygospores (Weiser and Muma 1966). These spores are often not observed in samples directly from the field according to the original description (Weiser and Muma 1966). However, later investigations suggested that resting spores may only be produced in locales and/or times of year where cold weather is common, which could be the reason they were not common in Florida when initially characterized (Carner 1976). These spores are ovoid to subspherical, with smooth to wrinkled cell three-layered wall (0.5μm) (Weiser and Muma 1966).
Neozygites Witlaczil is a genus of fungi that includes species that are obligate pathogens of mites and insects (Keller 1997;Montalva et al. 2014;Witlaczil 1885). Several species of Neozygites have been considered natural enemies of insect and mite pests, and have been investigated as potential biological control agents of economically important crops (Hajek and Delalibera 2009;Van der Geest et al. 2000). Neozygites was traditionally classified in the highly polyphyletic phylum Zygomycota F. Moreau based on morphological characters, such as coenocytic hyphae and zygospore production (Moreau 1954 ["1953"];Spatafora et al. 2016). In 2012, a new phylum Entomophthoromycota Humber was constructed to include all members of the Entomophthorales, previously placed in the incertae sedis subphylum Entomophthoromycotina Humber, which represented a monophyletic cluster unique from other fungal phyla (Humber 2012). In 2016, Neozygites and other zoopathogenic “zygomycete” fungi were classified into a new phylum Zoopagomycota Gryganskyi, M.E. Smith, Stajich & Spatafora, which was constructed to avoid taxonomic confusion between more specific, phyla-level names such as Basidiobolomycota Doweld (2001), Entomophthoromycota and Harpellomycota Doweld (2013) (Spatafora et al. 2016). All species of Neozygites remain in the order Neozygitales Humber (Humber 2012).
Neozygites includes 23 described species that have little phylogenetic resolution due to poor alignment with other Zoopagomycota species (Gryganskyi et al. 2013). The phylogenetic relationships of this genus are poorly resolved primarily to a lack of molecular data, which is due to the limitation of very few available in vitro cultures of this genus (Humber 2012). Species of Neozygites are difficult to culture due to complex nutritional requirements needed for growth (Delalibera et al. 2003;Duarte 2013). Currently, cultures are only available for species that infect mites (N. floridana, N. parvispora and N. tanajoae),although the aphid pathogen N. fresenii is the type species (Gryganskyi et al. 2013).
Neozygites floridana (J. Weiser & Muma) Remaud. & S. Keller was originally described as Entomophthora floridana, as a pathogen of the Texas citrus mite, Eutetranychus banksi McGregor, from Lake Alfred Florida in 1966 (Weiser and Muma 1966). Later Humber et al. suggestedconserving the widely published genus Triplosporium (Thaxter) Batko (1964) despite Neozygites being the older name (1885), and having priority over Triplosporium (Humber et al. 1981). Consequently, this nomeclatural conservation effort failed, but it is important to note to better understand the literature.
Neozygites floridana je grzib[3], co go nojprzōd ôpisoł Weiser & Muma, a terŏźnõ nazwã doł mu Remaud. & S. Keller 1980. Neozygites floridana nŏleży do zorty Neozygites i familije Neozygitaceae.[4][5] Żŏdne podgatōnki niy sōm wymianowane we Catalogue of Life.[4]
Neozygites floridana je grzib, co go nojprzōd ôpisoł Weiser & Muma, a terŏźnõ nazwã doł mu Remaud. & S. Keller 1980. Neozygites floridana nŏleży do zorty Neozygites i familije Neozygitaceae. Żŏdne podgatōnki niy sōm wymianowane we Catalogue of Life.
