Fungal Pathogens Of Aphids Spread With Host Dispersal Flight In The Low-Latitude Plateau Of Yunnan, China And Features Of Pandora Nouryi In Infective Biology

Aphids are global pests of crops and economic plants and are attacked by varieties of natural mortality agents, which include over 30 species of aphid-pathogenic fungi (mainly Entomophthorales). Aphid mycoses are considered one of classic pathogen-host interactions due to the well-known biology of aphid dispersal flight and dense colonies and the special epizootic features of main pathogens. This study sought to survey for the first time the resources of aphid-pathogenic fungi that occur in the low-latitude plateau of China-Burma border, to examine the potential of pathogen-infected, wasp-parasitized and healthy host alates in colonization, fecundity and mycosis transmission after immigration, and explore for the first time the infective and epizootiological features of obligate aphid pathogen Pandora nouryi found in the plateau. The results are given as follows.Pathogenic fungi and parasitoids of aphids present in air captures of migratory alates. To survey fungal pathogens and parasitoids of aphids in the low-latitude plateau of Yunnan, southwest China, 3553 migratory alates of Brevicoryne brassicae, Lipaphis erysimi, Myzus persicae were attracted to a yellow-plus-plant trap from air during a full-year period and individually reared on cabbage leaves for 7-14 days at 18-22℃and L:D 12:12. Among the trapped alates, 19.2% survived averagely for 2.3 (1-7) days before killed by 11 species of aphid-pathogenic fungi. Another 2.8% were mummified by the wasps Aphidius gifuensis, Diaeretella rapae, Ephedrus plagiator and Aphelinus mali after survival of 4.9 (3-13) days. Most of the mycosed alates (77.8%) were attributed to Entomophthorales predominated by Pandora neoaphidis (42.7%) and Zoophthora radicans (14.5%), followed by P. nouryi, Neozygites fresenii, Conidiobiolus spp., Entomophthora planchoniana and Z. aphidis at decreasing frequency. A mitosporic fungus, Lecanicillium lecanii, was found frequently in L. erysimi alates trapped in wet season. However, the B. brassicae alates captured in dry season were infected or parasitized very occasionally. Overall, the fecundity of the infected or parasitized alates before death warranted successful colonization on plants, though greatly reduced, and was well shown by the fitted probability for a given fecundity per capita and the increasing mean size of their progeny colonies. Contagious transmission of the alate-borne mycosis observed in most of the colonies caused high progeny mortalities within 14 days. The results highlight for the first time the diversity of aphid pathogens as well as the spread of both pathogens and parasitoids with host dispersal flight in the low-latitude plateau.Colonization potential of infected and parasitized alates trapped from air. Among the infected alates trapped from air, 83% became mycosed during colonization after trapping and a very few survived on day 6 or 7 with a mean (±SD) latent period of 2.30±1.26 days. All the parasitized alates averagely survived 4.89±1.94 days (with a few surviving for >7 days) before being mummified; wasp adults emerged from their mummies after developing for 5.6±1.3 days.The sizes of progeny colonies from the trapped alates generally increased over days after colonization but differed among the different groups. Overall mean (±SD) sizes of the colonies (no. nymphs per capita) from the infected alates increased from 2.0±2.0 (n=559) on day 1 to 35.4±51.3 (n=349) on day 14 for L.erysimi, 2.1±2.0 (n=119) to 72.1±76.5 (n=78) for M. persicae, and 4.4±3.7 (n=5) to 6.3±12.5 (n=5) for B. brassicae, respectively. The same observations from the parasitized alates of the three aphid species increased separately from 1.7±1.6 (n=58) to 86.6±73.7 (n=32), 1.3±1.40 (n=39) to 99.5±124.3 (n=22) and 0.7±1.1 (n=3) to 23.5±33.2 (n=3). In contrast, the progeny colonies of the alates free of both fungal infection and parasitism were conspicuously larger during the 14-day colonization, increasing from 2.6±2.0 (n=959) to 165.3±125.8 (n=381) for L. erysimi, 2.8±1.8 (n=605) to 180.3±114.4 (n=378) for M. persicae and 2.6±2.7 (n=260) to 69.7±64.5 (n=62) for B. brassicae.The fecundity of the infected or parasitized alates before death warranted successful colonization on plants, though greatly reduced, as was well shown by the fitted cumulative probability [P(m≤N)] for the alates producing≤m nymphs per capita and the increasing mean size of their progeny colonies. The relationship between m and P(m≤N) fit very well to a modified logistic equation for a given group of the alates or an aphid species (r²â‰¥0.988, P<0.001). Based on the fitted equations, healthy alates from air captures were highly capable of producing more nymphs than those infected or parasitized.Infective and epizootiological features of P. nouryi. Resting spore formation of some aphid-pathogenic Entomophthorales is important for the seasonal pattern of their prevalence and survival but this process is poorly understood. To explore the possible mechanism involved in the process, P. nouryi (obligate aphid pathogen) interacted with green peach aphid M. persicae on cabbage leaves under favorable conditions. Host nymphs showered with primary conidia of an isolate (LC₅₀: 0.9-6.7 conidia mm^-2 4-7 days post-shower) from air captures in the low-latitude plateau produced resting spores (azygospores), primary conidia or both spore types. Surprisingly, the proportion of mycosed cadavers forming resting spores (P_CFRS) increased sharply within the concentrations (C) of 28-240 conidia mm^-2, retained high levels at 240-1760, but was zero or extremely low at 0.3-16. The P_CFRS-C relationship fit well the logistic equation P_CFRS=0.6774/[1+exp(3.1229-0.0270C)] (r²=0.975). This clarified for the first time the dependence of in vivo resting spore formation of P. nouryi upon the concentration of infective inocula. A hypothesis is thus proposed that some sort of biochemical signals may exist in the host-pathogen interaction so that the fungal pathogen perceives the signals for prompt response to forthcoming host-density changes by either producing conidia for infecting available hosts or forming resting spores for surviving host absence in situ.In summary, 10 species of fungal pathogens were identified for the first time from the alates of three aphid species air-trapped in the low-latitude plateau with the discovery of full infection cycle of P. nouryi enriching our knowledge about Pandora species. Observations and modeling analysis have confirmed that both infected and parasitized alates were able to independently establish progeny colonies after immigration despite their reduced fecundity in comparison with that of healthy alates. Particularly, the alalte-borne mycoses were successfully transmitted to most of the progeny colonies. This further supports a hypothesis that both aphid pathogens and parasitoids may spread with host dispersal flight and provides deep insights into the biology of host flight. A new hypothesis for possible mechanisms involved in resting spore formation of Entomophthorales is proposed based on the first finding of the dependence of P. nouryi resting spore formation on the concentration of its primary conidia as inocula.