The versatility of simplicity: Structures of Cardiocephaloides longicollis used for different purposes during cercarial transmission

Integr Comp Biol. 2022 Jun 29;icac102. doi: 10.1093/icb/icac102. Online ahead of print.

Abstract

Transmission and infection strategies are critical for completing the life cycles of trematode parasites, which are characterized by complex life cycles involving multiple hosts and stages. Transmission between the first and second intermediate hosts typically relies on cercariae, a free-swimming larval stage that displays a series of behaviors to efficiently disperse, locate, attach to, and infect the next host. The aim of this study is to provide detailed information on behaviors used by furcocercariae (bifurcated tail) during its transmission from the snail to the fish host, using the laboratory-established model of Cardiocephaloides longicollis (Strigeidae). These cercariae are released from snails into seawater, where they swim, locate, penetrate the skin of fish, and encyst as metacercariae in their brain. In a series of in vivo assays, freshly-emerged cercariae were used to visually study their behavior and locomotion. Histopathology of experimentally infected gilthead seabreams with C. longicollis, taken at sequential post-infections times, were analysed to localize the migrating cercariae to the fish brain. Our results show that simplicity and versatility are the key features for the success of cercariae transmission by using their organs for different purposes. While 80% of the behavior was spent in a resting position, the most common swimming behavior was with tail-first, which is commonly described in furcocercariae to reach the host microhabitat. However, C. longicollis relies more on the furcae of the tail by using them as a propeller providing thrust and guidance when they swim, instead of using the tail stem. After attaching to the fish skin, cercariae rapidly creep on it using the oral- and ventral-suckers simulating a leech-like movement until they find a suitable penetration site. To penetrate, cercariae press the cephalic structures against the skin, while the ventral sucker anchors the cercariae to it. After this, they switch their locomotion to a slow peristaltic movement, opening the path through tissues with the help of their cephalic structures and anchoring their body with their surface spines. This is consistent with the post-penetration histological analyses, which suggested that C. longicollis cercariae move between the cells of the connective tissue and muscle fibers when migrating towards the fish's brain, without provoking relevant tissue damage or host responses. Understanding the versatility of cercarial structures to adapt to external conditions enriches our knowledge on parasites and their transmission ecology, opening the door to the design of avoidance methods in fish farms struggling with harmful parasites.

Keywords: cercariae behavior; larval stage; life cycle; multifunctional structures; parasite; transmission strategies.