Abstract
Some parasites are able to manipulate the behaviour of their hosts to their own advantage. One of the most well-established textbook examples of host manipulation is that of the trematode Dicrocoelium dendriticum on ants, its second intermediate host. Infected ants harbour encysted metacercariae in the gaster and a non-encysted metacercaria in the suboesophageal ganglion (SOG); however, the mechanisms that D. dendriticum uses to manipulate the ant behaviour remain unknown, partly because of a lack of a proper and direct visualisation of the physical interface between the parasite and the ant brain tissue. Here we provide new insights into the potential mechanisms that this iconic manipulator uses to alter its host’s behaviour by characterising the interface between D. dendriticum and the ant tissues with the use of non-invasive micro-CT scanning. For the first time, we show that there is a physical contact between the parasite and the ant brain tissue at the anteriormost part of the SOG, including in a case of multiple brain infection where only the parasite lodged in the most anterior part of the SOG was in contact with the ant brain tissue. We demonstrate the potential of micro-CT to further understand other parasite/host systems in parasitological research.
Highlights
The absurd behaviours of ants infected with larvae of the trematode, Dicrocoelium dendriticum (Rudolphi), were described by German parasitologists in the 1970’s4,5
Micro-CT revealed the internal anatomy of the ant host, as well as D. dendriticum metacercariae in the suboesophageal ganglion (SOG) and gaster (Fig. 2A)
These encysted metacercariae were unevenly distributed in the interior of the gaster, embedded between the cuticle and the hypodermal muscles and between the walls of the different portions of the digestive tract (Fig. 2B–D). 3D volume renderings showed several scar-like marks on the crop wall (Fig. 2D), likely produced during the penetration of cercariae following their ingestion
Summary
The absurd behaviours of ants infected with larvae of the trematode, Dicrocoelium dendriticum (Rudolphi), were described by German parasitologists in the 1970’s4,5. In a region of emergence in Cypress Hills Park in Alberta, Canada, infected ants (Formica aserva Forel) leave their nests during cool evenings to affix their mandibles onto the petals of flowers. This attachment to vegetation presumably facilitates the transmission of larval flukes into elk, deer, and beef cattle in this region[8]. Site-selection within the SOG cannot explain the attachment/detachment dichotomy, nor can it explain the long periods of apparently normal behaviour that occur when temperatures exceed 20 °C. Lee et al.[17] used CT and micro-CT virtual serial sections to visualise the host-parasite interface in the bronchi of dogs infected with adults of the lung fluke Paragonimus westermani Kerbert. Micro-CT methodology is becoming progressively more accessible to researchers combined with greatly improved resolution through the development of scanning systems capable of the submicron voxel size level[15]
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