Locomotion and attachment mechanisms of the respiratory mite Orthohalarachne attenuata

The respiratory mite Orthohalarachne attenuata, a parasite inhabiting the respiratory tract of otariid and odobenid pinnipeds, faces unique biomechanical challenges in its marine environment. It must securely attach to the slippery mucosa of its host while maintaining the ability to traverse dry and wet surfaces to recruit new hosts. This study explores the morphology of the attachment structures and mechanisms of O. attenuata larvae using scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM), high-speed video analysis, and centrifugal force measurements. Our findings confirm that, as in most Mesostigmata, the larvae of O. attenuata possess a specialized pretarsal structure consisting of two highly sclerotized claws and a soft, resilin-rich arolium; however, our analyses reveal specific morphological and functional adaptations of this structure related to attachment in the walrus nasal mucosa. Attachment strategy varies with substrate: the claws hook into soft walrus mucosa, whereas the arolium inflates to adhere to smooth surfaces. This dynamic interaction suggests a complex mechanism involving muscle control, flexible cuticle structures, leg positioning, and hemolymph pressure. Larvae employ a tripod gait pattern, facilitating agile movement across diverse surfaces. Force measurements on various substrates (dry and wet hydrophilic glass, hydrophobic plastics, polishing paper of various roughness properties, and walrus mucosa) demonstrate the highest attachment forces on walrus mucosa (safety factor: 348.95 ± 38.70) and wet glass (safety factor: 167.80 ± 119.09), underscoring the critical role of both claws and arolium in securing adhesion. These findings highlight the strong evolutionary adaptations of O. attenuata to its challenging environment and offer valuable insights for the development of bioinspired attachment systems suited for soft and wet substrates, particularly in marine applications.