Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods

Abstract

In this review, we describe water balance requirements of blood-feeding arthropods, particularly contrasting dehydration tolerance during the unfed, off-host state and the challenges of excess water that accompany receipt of the bloodmeal. Most basic water balance characteristics during the off-host stage are applicable to other terrestrial arthropods, as well. A well-coordinated suite of responses enable arthropods to conserve water resources, enhance their desiccation tolerance, and increase their water supplies by employing a diverse array of molecular, structural and behavioral responses. Water loss rates during the off-host phase are particularly useful for generating a scheme to classify vectors according to their habitat requirements for water, thus providing a convenient tool with potential predictive power for defining suitable current and future vector habitats. Blood-feeding elicits an entirely different set of challenges as the vector responds to overhydration by quickly increasing its rate of cuticular water loss and elevating the rate of diuresis to void excess water and condense the bloodmeal. Immature stages that feed on blood normally have a net increase in water content at the end of a blood-feeding cycle, but in adults the water content reverts to the pre-feeding level when the cycle is completed. Common themes are evident in diverse arthropods that feed on blood, particularly the physiological mechanisms used to respond to the sudden influx of water as well as the mechanisms used to counter water shortfalls that are encountered during the non-feeding, off-host state.

Fig. 1

The dynamics of water content during a blood feeding cycle in (A) adults and (B) immature stages. Note that the adult feeding cycle typically does not result in a net increase in water content, while a feeding cycle in immature stages (nymphs and larvae) results in a net increase in water content.

Fig. 2

Comparison of the water loss rates for off-host adult female hematophagous arthropods. Classification of xeric, mesic, and hygric is based on Hadley (1994). List in order from lowest to highest water loss rates: Rhodnius prolixus (Hemiptera; Hadley, 1994), Ornithodoros savigny (Argasidae; Hafez et al., 1970), Amblyomma cajennense (Ixodidae; Needham and Teel, 1991) Hyalomma dromedarii (Ixodidae; Hafez et al., 1970), Cimex lectularius (Hemiptera; Benoit et al., 2007b), Ornithodoros moubata (Argasidae Lees, 1947), Dermacentor andersoni (Ixodidae; Yoder et al., 2007), Amblyomma maculatum (Ixodidae; Yoder et al., 2009), Rhipicephalus sanguineus (Ixodidae; Yoder et al., 2006a), Glossina morsitans (Diptera; Bursell, 1960), Dermacentor variabilis (Ixodidae; Yoder et al., 2004), Dermacentor albipictus (Ixodidae; Needham and Teel, 1991), Amblyomma americanum (Ixodidae; Yoder et al., 2006c), Ixodes uriae (Ixodidae; Benoit et al., 2007a), Ixodes scapularius (Ixodidae; Yoder and Spielman, 1992), Ixodes ricinus (Ixodidae; Lees, 1946), Xenopsylla confromi (Siphonaptera; Fielden et al., 2002), Rhipicephalus annulatus (Ixodidae; Needham and Teel, 1991), Xenopsylla ramesis (Siphonaptera; Fielden et al., 2002), Ctenocephalides felis (Siphonaptera; Thiemann et al., 2003), Culex pipiens (Diptera; Benoit and Denlinger, 2007), Aedes aegypti (Diptera; Benoit et al., 2009), Aedes albopictus (Diptera; Benoit, J.B. unpublished observation), Anopheles arabiensis (Diptera; Gray and Bradley, 2005), Anopheles gambiae (Gray and Bradley, 2005).