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229 Discontinuous Ventilation in a Non-Insect, the Tick Amblyomma Marmoreum

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229 Discontinuous Ventilation in a Non-Insect, the Tick Amblyomma Marmoreum J. exp. Biol. 180, 229-245 (1993) 229 Printed in Great Britain © The Company of Biologists Limited 1993 DISCONTINUOUS VENTILATION IN A NON-INSECT, THE TICK AMBLYOMMA MARMOREUM (ACARI, IXODIDAE): CHARACTERIZATION AND METABOLIC MODULATION JOHN R. B. LIGHTON Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA LAURA J. FIELDEN Department of Zoology, University of the Witwatersrand, Private Bag 3, Wits 2050, Republic of South Africa and YIGAL RECHAV* Department of Microbiology, Medical University of South Africa, PO Medunsa 0204, Republic of South Africa Accepted 17 March 1993 Summary We examined and quantified the discontinuous ventilation cycle (DVC) characteristics of unfed nymphs and adults, as well as engorged nymphal and engorged diapausing and non-diapausing female adult life-stages, of the African tortoise tick Amblyomma marmoreum (Koch). All engorged stages ventilated continuously, with little evidence of active spiracular control. Unfed nymphs and adults ventilated discontinuously; at low activity and standard metabolic rate (SMR) levels, mean DVC duration was approximately 0.4h in nymphs (mean mass 0.7mg) and 2.8h in female adults (mean 21 21 mass 70mg). SMR, measured as rate of CO2 production (V˙CO·; 0.064 ml mg h and 0.019 ml mg21 h21, respectively), was almost tenfold lower than that estimated for spiders of equivalent mass. In adults, the DVC was modulated to accommodate changing V˙CO· chiefly by changes in DVC frequency. Modulation of other DVC characteristics was bimodal; at low V˙ CO· (below the ‘SMR threshold’), burst volumes were large and not correlated with V˙CO·, but the rate of CO2 emission during the burst was modulated by V˙CO·. Above the SMR threshold, burst volumes were small and tightly correlated with V˙CO·. No fluttering-spiracle phase could be detected, but CO2 bursts were triggered at low volumes above the SMR threshold, suggesting that hypoxia in addition to hypercapnia may initiate the termination of DVCs in the burst phase, rather than initiating the flutter phase as in insects. To explain this bimodal modulation of the DVC by V˙CO· (and hence V˙O·) above and below the SMR threshold, we hypothesize that, below the SMR threshold, unfed ixodid ticks – with their very low SMR and large surface area/volume ratio – may obtain significant amounts of O2 by transcuticular or other putative non- spiracular avenues of O2 uptake (larval ticks obtain all their O2 in this way). *Present address: Department of Biology, University of Bophuthatswana, Private Bag X 2046, Mmabatho 8681, Republic of South Africa. Key words: Amblyomma marmoreum, tick, ventilation, gas exchange, metabolism. 230 J. R. B. LIGHTON, L. J. FIELDEN and Y. RECHAV Introduction Apart from their impressive versatility as disease vectors, ticks have interested physiologists for many reasons, foremost among which is their capacity to withstand long periods between moulting and feeding. Ticks are ‘gorging–fasting’ organisms (Wharton, 1978) that usually spend more than 90% of their lives between blood meals, and can survive longer than any other arthropod without food or drinking water (for a review, see Needham and Teel, 1991). Their net water loss rates are accordingly very low, probably because of a cuticular lipid barrier (see Sonenshine, 1991) and the ability of many species to sequester water from subsaturated air (Knülle and Devine, 1972; Rudolph and Knülle, 1974). Stringent spiracular control is also presumably important in restricting water loss. Ticks are unusual among tracheate arthropods in possessing only one pair of spiracles (see Sonenshine, 1991, for a description). These spiracles are very complex and many aspects of their structure and function remain obscure or controversial, in particular their opening and closing mechanisms (Sonenshine, 1991; Knülle and Rudolph, 1982) and the possible role of the spiracular plate in retarding water loss (Pugh et al. 1988; but see Pugh et al. 1990). However, like insect spiracles, tick spiracles open at high CO2 concentrations (Mellanby, 1935). If the spiracles are forced to stay open in this fashion, overall water loss rates increase considerably (Hefnawy, 1970; Rudolph, 1976). More relevant to natural conditions, in an ambitious experiment similar to Kestler’s (1978, 1980, 1985 and unpublished) pioneering measurements of water loss rate during insect ventilation, Rudolph and Knülle (1979) demonstrated intermittent bouts of rapid mass loss in female ticks (Amblyomma variegatum), which they assumed to be synchronous with spiracular opening episodes. They also demonstrated that isolated spiracles held in Ringer’s solution will open and close at predictable CO2 concentrations. This amounts to strong inferential evidence of discontinuous CO2 release, roughly equivalent to the insect discontinuous ventilation cycle or DVC, in a non-hexapod arthropod. In this paper we confirm the existence of discontinuous CO2 release in a tick (Amblyomma marmoreum Koch) by direct measurement and characterize its variation across two of the tick’s three active life stages (the first or larval stage of most ticks lacks tracheae altogether and presumably ventilates by diffusion; Needham and Teel, 1986). Amblyomma marmoreum is a hard-bodied or ixodid tick. Almost all tick disease vectors belong to the family Ixodidae, which differ from soft-bodied or argasid ticks chiefly in possessing a hardened dorsal scutum and the habit of feeding only three times in their lives, with some exceptions. After emerging from the egg, the larval ixodid tick feeds once on a primary host, then drops off and moults into a nymphal tick, which also feeds just once before again dropping off the host. The nymphal tick moults into a ‘flat’ or pre-feeding adult, which searches out prey, generally quite specific to the species (the previous two stages are more catholic in host selection). Once on the host, the adult female tick becomes highly engorged, feeding from a blood pool that gathers beneath her barbed mouthparts, which are set into the host with a secreted cement. Finally, the engorged female drops off, after having consumed as much as 8cm3 of blood (Balashov, 1972), and, after an optional diapause in many species, produces large quantities of eggs – Tick ventilation 231 38000 or more in some Amblyomma species (Dipeolu and Ogunji, 1980) – which are expelled from the anterior of her idiosoma or unsegmented body. She then dies. Amblyomma marmoreum is a typical representative of its genus, being larger than most ixodid ticks and considered to be close to ancestral forms that evolved in the late Paleozoic to early Mesozoic eras, when reptiles first appeared (see Hoogstraal, 1985). Indeed, Amblyomma marmoreum, like many of its congeners, still attacks reptiles. Although larvae and nymphs exhibit wide host preferences (such early hosts may be very mobile and assist in the dispersion of the species) adults are almost invariably ectoparasites of tortoises (Norval, 1975; Fielden et al. 1992). Females may, as in other Amblyomma species, oviposit soon after dropping from the host (typical egg production approximately 12000; Fielden et al. 1992). If temperatures are high, as in mid-summer, a variable delay or diapause may occur before oviposition (Fielden et al. 1992). Materials and methods Animals Ticks used in this investigation were from laboratory stocks (flat stages) or were collected from or in the vicinity of tortoises (Geochelone pardalis) maintained in an animal care facility at the Biology Department of the Medical University of South Africa. All appropriate animal care regulations were followed. Ticks were transferred to a laboratory at the Physiology Department of the University of Witwatersrand Medical School in Johannesburg for measurement. Engorged nymphs and non-diapausing engorged adults had dropped from their hosts 2–4 days prior to measurement. Diapausing engorged females had dropped from their hosts approximately 30–45 days before measurement. Respirometry We employed flow-through respirometry utilizing a Sable Systems TR-2 respirometry system (Sable Systems, 476 E South Temple, Salt Lake City, UT 84111), respirometers of 5–20cm3 volume, computer-controlled baselining, and flow rates of 50–100cm3 21 min STPD. All H2O and CO2 was scrubbed from the incurrent air stream by a Drierite/Ascarite/Drierite column, and the excurrent air was dried by a low-volume magnesium perchlorate scrubber before passing through the CO2 analyzer. Details of the techniques have been published elsewhere (Lighton, 1990, 1991a,b, 1992; Lighton et al. 1993). We monitored flat ticks for 10–20h at a temporal resolution of 5–10s. Engorged ticks ventilated essentially continuously and could be characterized fully in a single recording of 40min duration at a temporal resolution of 1s. Computer records of CO2 21 production (V˙CO·) were converted to ml CO2 h for analysis. Areas under CO2 bursts were determined by integration against time in hours, yielding volume in ml. Respiratory quotients (RQ) were determined by a closed-system technique described elsewhere (Lighton, 1991a). All measurements were made in an air-conditioned laboratory at 23±1˚C. Statistics Means are accompanied by sample sizes (N) and standard deviations. Regressions were 232 J. R. B. LIGHTON, L. J. FIELDEN and Y. RECHAV determined by least squares, with significance testing by analysis of variance (ANOVA), and compared by analysis of covariance (ANCOVA). Means were compared using Student’s t-test. Results Results are summarized in Tables 1–4. In all cases, V˙CO· (and V˙O·) were very low compared to values expected from similar-sized insects or spiders (see Discussion). The dramatic changes of mass and V˙CO· between life-stages are summarized in Table 5. Ventilation characteristics None of the engorged nymphs or adults ventilated discontinuously (Fig. 1). Ventilation of the engorged stages was somewhat variable, with a coefficient of variation (CV, which is standard deviation divided by mean) of about 0.3 over an interval of approximately 40min. However, variations in ventilation were chaotic and of short duration, and CO2 never dropped below about 25% of the mean value.
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