Herpomyces ectoparasitic fungi (Ascomycota, Laboulbeniales) are globally distributed by their invasive cockroach hosts and through the pet trade industry

ABSTRACT

The introduction of non-native animals occasionally results in the co-introduction of their microbial symbionts or parasites. The trade of exotic pets and zoo animals has inadvertently introduced several parasitic species to countries where they are non-native. Both the presence of suitable native hosts and opportunity for dispersal determine whether these non-native species become naturalized. During our studies dealing with species of Herpomyces (Ascomycota, Laboulbeniomycetes), fungi that are exclusively ectoparasitic on cockroaches (Hexapoda, Blattodea), we make use of artificial colonies. Most of our specimens originate from pet stores and laboratory populations. Although they were originally intended for transmission studies, we discovered that some cockroaches from artificial colonies carried fruiting bodies of Herpomyces. We screened a total 292 cockroaches from 11 populations that we maintained after purchase. Sources were different pet stores, a toxicological laboratory, and a biological supply company. In eight populations, we found at least some Herpomyces-infected cockroaches. Parasite prevalence varied between 8.77% and 86.33%. Host associations were Blatta orientalis with Herpomyces stylopygae, Blattella germanica with H. ectobiae, Periplaneta americana with H. periplanetae, Phoetalia pallida with H. leurolestis, and Shelfordella lateralis with an undescribed species of Herpomyces. Apart from the new reports, host associations, and consequences for taxonomy (a new species based on morphological and molecular characters), we started to think about the geographic distributions of these fungi and how we, humans, shape them through spreading hosts and through international pet trade. We reviewed the currently known records of Herpomyces-associated cockroaches and host-parasite relationships. Based on the available data, on a global scale, at least half of the currently known species of Herpomyces are spread by globally invasive host species and through international pet trade. This indicates that the distribution and host range of these obscure and often unnoticed fungi are affected by human activities.

KEYWORDS:

• Fungal parasite
• distribution
• invasive species
• laboratory animals
• pet trade

ACKNOWLEDGMENTS

The authors thank József Schmidt for providing B. germanica and B. orientalis samples. The authors are grateful for Heidi Hopkins (Species File Group, University of Illinois Urbana-Champaign) for her excellent input with cockroach nomenclature and taxonomy and for commenting on a previous version of the manuscript.

D.H. wants to take the opportunity to specifically acknowledge Dr. Meredith Blackwell for being an inspiration for young, aspiring mycologists. Several years ago, in 2009, I contacted her and while I was just a simple, starting bachelor student at the time, she went far and wide to provide me with the answers I needed. She is a prime example of a researcher who is not shy to help or share data and, because of this, sets the bar high for other PIs, professors, and senior researchers.

Supplemental data

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Notes

¹ Taxonomic authorities for all fungal and insect taxa are provided in SUPPLEMENTARY TABLE 2.

Additional information

Funding

W.P.P. was supported through the ÚNKP-16-4-IV New National Excellence Program of the Ministry of Human Capacities of Hungary. A.T. and F.B. were supported by the “AntLab” Marie Curie Career Integration Grant, part the 7th European Community Framework Programme. T.W.W. acknowledges the Harvard College Research Program, for supporting his senior thesis work on Herpomyces (2015–2016).