A comparison of the cuticular properties of argasid and ixodid ticks: Ornithodoros moubata (Argasidae) vs. Amblyomma heb

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A comparison of the cuticular properties of argasid and ixodid ticks: Ornithodoros moubata (Argasidae) vs. Amblyomma hebraeum and Ixodes pacificus (Ixodidae) Peter C. Flynn1   · Jan Hendrik Forth2 · W. Reuben Kaufman3,4 Received: 21 August 2020 / Accepted: 2 November 2020 © Springer Nature Switzerland AG 2020

Abstract Ticks (Chelicerata, Ixodida) are blood-feeding ectoparasites believed to have evolved at least about 120 millions of years ago and found worldwide. However, many aspects of their unique life cycle and anatomy, including their mechanical properties, remain to be understood. Here, we compared the mechanical properties of the cuticle of the argasid tick Ornithodoros moubata to those of two species of ixodid tick, Amblyomma hebraeum and Ixodes pacificus that we explored in our earlier studies of the tick exoskeleton. Significant differences were expected given the substantial difference in life cycle, including a five-fold increase during the repeated adult blood meal for female O. moubata vs. 70- to 120-fold during the single feeding of the adult female A. hebraeum and I. pacificus. We demonstrate here that the layered structure and mechanical properties (stiffness and viscosity) of the cuticle show minor differences, but the difference in cuticle thickness is substantial. Ductility is lost during feeding; reduced pH restores ductility. Previous work suggests that this occurs in vivo in engorged ixodid ticks; there is no evidence of this occurring in vivo in O. moubata. Thinning of cuticle in O. moubata fed females is consistent with the predicted stretch of cuticle due to the blood meal; there is no evidence of cuticle synthesis during the short feeding period. Dimensional analysis suggests that the soft feel of argasid ticks is related to cuticle thickness, not cuticle stiffness. Relative to argasid ticks, the hard ixodid ticks accommodate a ca. 20-fold higher size of blood meal by starting with a thicker cuticle and growing much additional cuticle during engorgement. Keywords  Ornithodoros moubata · Ixodes pacificus · Amblyomma hebraeum · Argasidae · Ixodidae · Cuticle

* Peter C. Flynn [email protected] 1

Department of Mechanical Engineering, University of Alberta, Edmonton T6G 2E9, Canada

2

Friedrich-Loeffler-Institut, Südufer 10, 17493 Greifswald, Insel Riems, Germany

3

Department of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada

4

Present Address: Gulf Island Veterinary Clinic, Salt Spring Island, BC, Canada



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Experimental and Applied Acarology

Introduction The ticks (Ixodida) comprise three families: Ixodidae (more than 700 species), Argasidae (about 200 species), and Nuttalliellidae (only one species) (Barker and Murrell 2008; Mans et al. 2019). Ixodid ticks are commonly known as hard ticks, based on their feel relative to the far more flexible and compliant argasid ticks, the soft ticks. Nuttalliella namaqua is thought to be an early offshoot of the ancestral Ixodida lineage (Mans et al. 2011). Few specimens have been collected, b