First evidence for a possible invasional meltdown among invasive fish parasites

S. Emde,S. Klimpel,M. A. A. Hohenadler,B. Sures,K. I. Honka

doi:10.1038/s41598-018-33445-4

Abstract

Biological invasions are frequently studied topics in ecological research. Unfortunately, within invasion ecology parasite-associated aspects such as parasite impacts on new environments and on local host populations are less well-studied. Round gobies migrating from the Ponto-Caspian region into the Rhine River system are heavily infested with the Ponto-Caspian acanthocephalan parasite Pomphorhynchus laevis. As shown by experimental infestations the acanthocephalans occur as pre-adults in host-encapsulated cysts within the internal organs of the migrating gobies, but remain infective for their definitive host chub. Recently, we described the occurrence of larvae of another parasite, the invasive eel swim bladder nematode Anguillicola crassus, in these Pomphorhynchus cysts. In the present study, we could prove the infectivity of the nematode larvae for European eels for the first time. After experimental inoculation of Pomphorhynchus cysts occasionally infested with A. crassus larvae, the nematodes grow to maturity and reproduce whereas all P. laevis were unviable. We therefore postulate that the nematode larvae behave like immunological hitchhikers that follow a “Trojan horse strategy” in order to avoid the paratenic host’s immune response. Accordingly, the interaction between both invasive parasites gives first evidence that the invasional meltdown hypothesis may also apply to parasites.

Highlights

Invasion of free-living organisms and their effects on new habitats has emerged as a major threat for ecosystems around the globe, partly with irreversible consequences for the local biota
Hyperparasitized cysts – what in detail describes acanthocephalan cysts that were simultaneously infested by P. laevis and A. crassus - which were gathered from N. melanostomus individuals from the Rhine River demonstrated that A. crassus frequently enters the cyst most likely to avoid immune responses of the paratenic host
The present study demonstrates for the first time that larvae of A. crassus, enclosed in the cysts of encapsulated P. laevis, remain able to infest their definitive host, the European eel

Summary

Introduction

Invasion of free-living organisms and their effects on new habitats has emerged as a major threat for ecosystems around the globe, partly with irreversible consequences for the local biota. Many nonindigenous species were able to establish in the Rhine River over the past decades, invaders from water bodies of the Ponto-Caspian region were among the most successful[22] Species such as the amphipod Dikerogammarus villosus or the fish species Neogobius melanostomus or Ponticola kessleri usually become dominant species in newly invaded areas due to their invasion strategy that provide them with competition advantages against local species[23,24]. Recent research has shown that cysts of P. laevis in N. melanostomus may contain larvae of another invasive parasite species, Anguillicola crassus[31] This nematode causes severe health impacts for the native eel species in Europe[32,33]. In order to test the viability and infectivity of encapsulated A. crassus larvae, we conducted an infection experiment where European eels were inoculated with cysts collected from Ponto-Caspian gobies

Methods

Results

Conclusion