4309.pdf ALCES VOL. 43, 2007 MUSANTE ET AL. - METABOLIC IMPACTS OF WINTER TICKS 101 METABOLIC IMPACTS OF WINTER TICK INFESTATIONS ON CALF MOOSE Anthony R. Musante, Peter J. Pekins, and David L. Scarpitti Department of Natural Resources, University of New Hampshire, Durham, NH 03824, USA ABSTRACT: Moose (Alces alces) are susceptible to late winter mortality from infestation of winter ticks (Dermacentor albipictus) throughout much of North America. Calves, perhaps more so than other ages of moose, likely experience chronic, and eventually acute anemia from blood removal by adult female ticks that peaks during weeks 4 – 6 of the 8-week engorgement period. We modeled the potential metabolic impact on protein and energy balance of moose calves associated with blood loss during four levels, low to severe, of winter tick infestation. Our conservative estimates indicated that total blood loss in weeks 4 – 6, as a percent of total blood volume, ranged from 27 to 48% and 64 to 112% during moderate (30,000 ticks) and severe (70,000 ticks) infestations, respectively. The percent of the daily metabolizable energy requirement needed to replace daily blood loss during weeks 4 – 6 was 4.9 – 8.2% and 11.4 – 19.2% during moderate and severe infestations, respectively. The protein protein loss during weeks 4 – 6 was 29 – 49% and 68 – 114% of the daily protein requirement in continuous weeks. Energy costs associated with compensating for blood loss would likely elevate the increased physiological stress related to concurrent anemia. Severely infested calves are obviously susceptible to late winter mortality, and the impact of moderate infestations would be exacerbated by secondary parasitic infestations, severe winters, and poor body condition. ALCES VOL. 43: 101-110 (2007) Key words: Alces alces, anemia, blood loss, Dermacentor albipictus, energy, infestation, moose calves, mortality, protein, winter ticks Moose (Alces alces), elk (Cervus elaphus), and white-tailed deer (Odocoileus virginianus) are the three main hosts of the winter tick (Dermacentor albipictus) in North America. Moose are the most severely affected from infestations of winter ticks that cause hair loss and damage (McLaughlin and Addison 1986, Samuel 1991), excessive grooming (Mooring and Samuel 1999), chronic weight loss (Glines and Samuel 1989, Addison et al. 1994), and reduced growth and fat stores (McLaughlin and Addison 1986). No reduction in food intake (Addison and McLaughlin 1993) and only one case of tick-induced anemia have been reported for captive moose (Glines and Samuel 1989, Addison et al. 1998b); however, these consequences are more likely to occur in wild moose. Substantial mortality associ- ated with severe tick infestations has occurred throughout much of North American moose range (Samuel 2004). Winter tick related mortality was responsible for 41% (n = 16) of radio-marked mortality in New Hampshire with calves representing 88% of deaths (Mu- sante 2006), although all age classes of moose have been associated with winter tick-related mortality (Samuel and Barker 1979, Pybus 1999, Samuel and Crichton 2003). Presum- ably, the large volume of blood loss associated with severe tick infestations further reduces nutritional status during March – April when - cit (Glines and Samuel 1989, Samuel 2004). Calves are likely the most susceptible cohort METABOLIC IMPACTS OF WINTER TICKS - MUSANTE ET AL. ALCES VOL. 43, 2007 102 and anemia is suspected as the primary factor of mortality. - ing a 9 – 10 week period in late February to mid-May, peaking in late March – early April feeding for several species of adult female ixodid (hard body) ticks ranges from 6 to 13 days and blood removal can equal 3.0 – 7.5 times their engorged body weight (Sonenshine engorgement is completed within several days with a large volume of blood loss dur- ing the last 24 – 36 hours of feeding. Blood concentration in the cattle tick (Boophilus microplus) is greatest during the last hours - sumed a concentrated blood meal twice their own weight (Seifert et al. 1968). blood removal by ectoparasites has been Roby et al. 1992, Simon et al. 2003), reptiles (Wikelski 1999), small mammals (Khokhlova et al. 2002), and livestock (Seifert et al. 1968, Springell et al. 1971, Corrier et al. 1979, Norval et al. 1988). These studies indicated that blood consumption by parasites has varying effects on blood protein, weight gain, behavior, productivity, and metabolic rate of hosts. Studies have been conducted involving energetic consequences of tick-induced hair loss and grooming in moose (McLaughlin and Addison 1986, Samuel 1991, Mooring and Samuel 1999); however, little research exists on the relationships among tick infes- tation, blood loss, and metabolic balance in wild ungulates. The link between tick infestation and mortality of moose calves is evident; how- ever, the physiological impact on their energy and protein balance has not been estimated quantitatively. Such estimates are useful to understand and predict mortality associated with winter tick infestations. The objective of this study is to estimate the impact of blood loss from winter tick infestations on energy and protein balance of moose calves. METHODS Metabolic impacts of blood loss were esti- mated with models that incorporated variable calf weights, levels of tick infestation, weight of engorged ticks, and timing of feeding. Calf weight in March – April was set at 150 and 175 kg (Samuel 2004), although weights of 11-month-old captive calves may exceed 200 kg (Addison et al. 1994, Broadfoot et al. 1996). Tick infestation level was set as 10,000 (low), 30,000 (moderate), 50,000 (high), and 70,000 (severe) ticks (W.M. Samuel, University of Al- berta, personal communication). The number of adult females at each infestation level was estimated as 25.6% of the total tick load as measured on calves in March – April (Samuel 2004). Larvae, nymphs, and adult males were not considered in the analysis, because adult males consume relatively little blood com- pared to adult females (Sonenshine 1991); and unfortunately, similar data about immature life stages is limited (W.M. Samuel, University of Alberta, personal communication). Mean engorged weights of adult female ticks have been estimated at 0.61 (Glines 1983) and 0.85 g (Addison et al. 1998a); we used the same conservative estimate of 0.50 g as Samuel (2004) to account for ticks not fully engorged due to early removal by grooming all adult female ticks fed on this amount of blood. Total amount of blood loss per adult weight because undigested blood can be 2X 1991); therefore, blood loss was estimated as 2 and 3X engorged weight. Using moose calves experimentally infested with 30,000 that tick drop-off occurred primarily from March to April, peaking between 20 March and 6 April. In the current study the drop-off ALCES VOL. 43, 2007 MUSANTE ET AL. - METABOLIC IMPACTS OF WINTER TICKS 103 period and total blood loss was estimated over an 8-week period between 1 March and 25 April; proportional blood loss was estimated as 15% in weeks 0 – 2, 25% in weeks 2 – 4, 50% in weeks 4 – 6, and 10% during weeks 6 – 8. Vertebrate blood contains approximately 15% hemoglobin and 7% plasma proteins (Sonenshine 1991). Hemoglobin and total protein in blood of moose calves during late winter average 0.17 and 0.06 g/mL, respec- tively (Franzmann and LeResche 1978). We assumed a conservative value of 0.20 g protein/mL of blood, 4.3 kcal/g protein (Schmidt-Nielson 1997), and a metabolic ef- 1989); energetic cost of replacing blood was protein requirements were assumed as 168 and 189 g protein/day for 150 and 175 kg calves, respectively (Schwartz et al. 1987, Robbins 1993). Total blood volume was estimated as 8% of body weight (see Samuel 2004); calves weighing 150 and 175 kg had blood volumes of 12,000 and 14,000 mL, respectively. The daily metabolizable energy requirement for maintenance of a calf was assumed as 134 kcal/kg0.75/d (Cool and Hudson 1996), which equaled 5,743 and 6,447 kcal/d for a 150 and 175 kg calf, respectively. RESULTS Total blood loss at the low infestation level (10,000 ticks) was estimated as 2,560 and 3,840 mL for 2 and 3X engorged weight, respectively; total blood loss at the severe in- festation level (70,000) was 17,920 and 26,880 mL, values exceeding total blood volume (Fig. 1). Percent total blood volume lost in 150 and 175 kg calves with low, moderate, high, and severe infestations ranged from 21 to 224% and 18 to 192%, respectively; percent daily blood loss ranged from 0.4 to 4.0% and 0.3 to 3.4%, respectively (Table 1). Percent total blood volume lost in 150 and 175 kg calves with low to severe infestations during weeks 4 – 6 ranged from 11 to 112% and 9 to 96%, respectively; percent daily blood loss ranged from 0.8 to 8.0% and 0.7 to 6.9%, respectively (Table 1). The energy cost to replace blood loss ranged from 2,944 to 20,608 kcal at 2X en- gorged weight at the four levels of infestation, and 4,416 to 30,912 kcal at 3X engorged weight 0 5000 10000 15000 20000 25000 30000 10,000 30,000 50,000 70,000 Tick Infe station Le v e l B lo o d L o ss (m L ) 2X blood-fed weight 3X blood-fed weight Total blood volume (150 kg calf) Fig. 1. Total blood removal by adult female winter ticks at low to severe infestation levels on moose calves over the 8-week engorgement period. Calf Weight (kg) 150 175 Infestation 100% 50% 100% 50% Level Week Week Week Week 0-8 4-6 0-8 4-6 10,000 2X 21 (0.4) 11 (0.8) 18 (0.3) 9 (0.7) 3X 32 (0.6) 16 (1.1) 27 (0.5) 14 (1.0) 30,000 2X 64 (1.1) 32 (2.3) 55 (1.0) 27 (2.0) 3X 96 (1.7) 48 (3.4) 82 (1.5) 41 (2.9) 50,000 2X 107 (1.9) 53 (3.8) 91 (1.6) 46 (3.3) 3X 160 (2.9) 80 (5.7) 137 (2.4) 69 (4.9) 70,000 2X 149 (2.7) 75 (5.3) 128 (2.3) 64 (4.6) 3X 224 (4.0) 112 (8.0) 192 (3.4) 96 (6.9) Table 1. Total and daily percent blood volume of calf moose removed by engorging adult female ticks. Infestation level, stage, engorged weight (2 and 3X), and calf weight were varied; total blood volume was estimated as 8% of body weight. METABOLIC IMPACTS OF WINTER TICKS - MUSANTE ET AL. ALCES VOL. 43, 2007 104 budget for a 150 kg calf ranged from 0.9 to 9.6% for low to severe infestations over 8 weeks, and 1.8 to 19.2% during weeks 4 – 6; the estimates for a 175 kg calf were 0.8 – 8.6% and 1.6 – 17.1%, respectively (Table 2). Total protein lost during low-to-severe infestations ranged from 512 to 3,584 and 768 to 5,376 g at 2 and 3X blood-fed weight, moderate infestation level (30,000) and 2-3X blood-fed weight was 11.0 – 16.5 g during weeks 6 – 8 and 54.9 – 82.3 g during weeks 4 a severe infestation peaked during weeks 4 – 6 and exceeded the daily protein requirement of 150 and 175 kg calves; daily protein loss was 50 – 100% of the daily protein requirement during weeks 2 – 6 (Fig. 4). As a percent of the daily protein requirement during weeks 4 – 6, protein loss of a 150 kg calf peaked at 33 – 49% at a moderate infestation level, and 76 – 114% at a severe infestation level; protein loss of a 175 kg calf peaked at 29 – 44% and 68 – 102% in moderate and severe infestations, respectively (Fig. 4). DISCUSSION This exercise, performed with conserva- tive estimates, indicated that blood loss as- sociated with moderate to severe infestations of ticks has substantial impact on energy and protein balance in moose calves. The physiological impact of blood removal by adult female ticks extends for approximately 8 weeks, and calves likely experience chronic, and eventually acute anemia during peak engorgement by weeks 4 – 6 during early to mid-April. Although anemia associated with blood removal by ticks is well recognized in cattle (Francis 1960, O’Kelly and Seifert 1969, Corrier et al. 1979), there is little to no evidence in captive moose (Glines and Samuel 1989, Addison et al. 1998b). Nevertheless, anemia is hypothesized in tick-infested wild moose. Hemorrhagic anemia caused by parasites occurs when the balance between blood loss and production is not maintained, and calves are unable to compensate for blood loss. The protein loss estimates in this study indicate that the potential for hemorrhagic anemia is greatest in weeks 4 – 6 (Fig. 4). As a consequence of their age and smaller body size, calves have higher meta- bolic demands than adults on a relative scale 0 5000 10000 15000 20000 25000 30000 35000 10,000 30,000 50,000 70,000 Tick Infe station Le v e l E n er g y C o st (k ca l) 2X blood-fed weight 3X blood-fed weightDaily energy requirement (150 kg calf) Fig. 2. Total energy cost for moose calves to replace blood loss at low to severe infestation levels of adult female winter ticks over the 8-week engorgement period. Calf Weight (kg) 150 175 Infestation 100% 50% 100% 50% Level Week Week Week Week 0-8 4-6 0-8 4-6 10,000 2X 0.9 1.8 0.8 1.6 3X 1.4 2.7 1.2 2.4 30,000 2X 2.7 5.5 2.4 4.9 3X 4.1 8.2 3.7 7.3 50,000 2X 4.6 9.2 4.1 8.2 3X 6.9 13.7 6.1 12.2 70,000 2X 6.4 12.8 5.7 11.4 3X 9.6 19.2 8.6 17.1 Table 2. The cost of replacing blood removed by engorging adult female ticks as a percent of the daily metabolizable energy requirement of moose calves. Infestation level, stage, engorged weight (2 and 3X), and calf weight were varied; total blood volume was estimated as 8% of body weight. ALCES VOL. 43, 2007 MUSANTE ET AL. - METABOLIC IMPACTS OF WINTER TICKS 105 (Schwartz et al. 1991). Stored body fat and protein allow moose to survive normal en- Renecker 1998); however, calves are more susceptible to late winter mortality, because they have proportionally less body fat than adults (Van Ballenberghe and Ballard 1998). of minimal nutritional value (Schwartz and Renecker 1998) and the relative energetic cost associated with compensating for blood loss is presumably higher for animals in poor condition, especially calves. Moose calves severely infested or in weakened condition are probably unable to sustain the energetic demand for blood regeneration and consump- tion of adequate food resources. Volume of daily blood loss was an important factor in the mortality of smaller, tick-infested livestock calves compared to larger surviving calves (Corrier et al. 1979). Tick-infested moose calves that are heavier possibly have a bet- ter likelihood of recovery and survival from blood loss. Calves in poor condition may also experience more pronounced energy and which likely groom more and should remove a greater number of ticks. The daily percent loss of total blood volume during weeks 4 – 6 ranged from 2.0 to 3.4% and 4.6 to 8.0%, respectively, during moderate and severe tick infestations of 30,000 and 70,000 ticks (Table 1). Calves infested with 50,000 ticks would lose 1 – 2X their blood volume over the 8-week engorgement period. Guidelines for blood collection of healthy animals on an adequate nutritional plane suggest that 10% of blood volume can be removed every 3 – 4 weeks or 1% daily for repeated bleeds at shorter intervals (Morton et al. 1993). Further, total blood loss as a percent of total blood volume during weeks 4 – 6 ranged from 27 to 48% and 64 to 112%, respectively (Table 1). Most animals experi- ence hemorrhagic shock if 30 – 40% of blood volume is removed over a short period of time, and Rowan 1989). The percent of the daily metabolizable energy requirement required to replace the average daily blood loss during the engorge- ment period ranged from 2.4 to 4.1% and 5.7 to 9.6% in moderate and severe infestations (Table 2). However, the daily estimates were twice that during weeks 4 – 6 (Table 2), and these additional energy costs would increase - ter, accelerate nutritional decline and weight loss, and likely cause increased physiological stress related to concurrent anemia. Calves normally experience a negative energy bal- ance in winter when the metabolizable energy requirement exceeds forage intake energy; 40% in winter assuming availability of quality dry matter forage (2.2 kcal/g of metabolizable energy) and a daily consumption rate of 1% body weight (Schwartz and Renecker 1998). 0 1000 2000 3000 4000 5000 6000 10,000 30,000 50,000 70,000 Tick Infe station Le v e l P ro te in L o ss (g ) 2X blood-fed weight 3X blood-fed weight Daily protein requirement (150 kg calf) Fig. 3. Total protein cost for moose calves to re- place blood loss to adult female winter ticks at low to severe infestation levels over the 8-week engorgement period. 0 25 50 75 100 125 150 175 200 Week 0-2 Week 2-4 Week 4-6 Week 6-8 Engorgement Period P ro te in (g ) 70,000 ticks 2-3X blood- fed weight 30,000 ticks 2-3X blood- fed weight 175 kg 150 kg 100% 50% Daily p rotein requirement - ated with blood loss at moderate and severe infestation levels of adult female winter ticks over the 8-week engorgement period. METABOLIC IMPACTS OF WINTER TICKS - MUSANTE ET AL. ALCES VOL. 43, 2007 106 Calves infested with 70,000 ticks would lose an equivalent of 3 – 5 days of metabolizable energy requirement over the 8-week engorge- ment period. Increased grooming and reduced feeding during March – April accentuate the negative energy balance at the end of winter (McLaughlin and Addison 1986, Samuel 1991, Mooring and Samuel 1999). Although the role of protein metabolism may have the strongest cost associated with blood replacement adds to the negative impact of ticks. Low, moderate, and heavy tick numbers had minimal effect on hematological param- eters of captive moose maintained on a 16% protein diet (Addison et al. 1998b); however, winter browse typically has 5 – 7% protein and is poorly digested (Schwartz and Renecker 1998). Conversely, poor nutrition reduced hematological values of cattle lightly infested with Boophilus microplus compared to those on an adequate diet (O’Kelly et al. 1971), and tick-infested cattle had lower concentrations of hemotacrit, hemoglobin, serum albumin, and total protein than tick-free cattle (O’Kelly and Seifert 1969). Alexander and Kiesel (1965) report that blood loss coupled with low protein diet (8%) adversely affected weight gain, hemoglobin, and hematocrit in lambs; minimal effects occurred in lambs maintained on a 16% protein diet. Thus, the negative impact and host-susceptibility of parasitism in ruminants are greater in malnourished animals; adequate nutrition and protein intake reduce impact (Van Houtert and Sykes 1996, Coop and Kyriazakis 2001). loss and regeneration is probably the most critical physiological problem for calves. In severely infested moose calves occurred for 4 continuous weeks (weeks 2 – 6; Fig. 4). Losses were most pronounced during weeks 4 – 6; 29 – 49% in a moderate infestation and 68 – 114% in a severe infestation (Fig. 4). Calves infested with 70,000 ticks would lose an equivalent of 3 – 4 weeks of the daily protein requirement. Moose are invariably - ing winter (Schwartz et al. 1988); therefore, compensation would be problematic, because the engorgement period occurs prior to spring green-up when quality and quantity of forage are limited. Calves experiencing severe blood loss should be considered high-risk mortality from anemia and associated effects. Their ability to survive tick infestations is probably the level of infestation. The estimated proportion of adult female ticks on adult moose during late winter is lower on cows (18.0%) and slightly higher on bulls (27.6%), relative to calves (25.6%) (Samuel 2004). Based on similar calculations as with associated with a severe infestation level is 4.5 – 6.7% for a cow (360 kg) and 6.3 – 9.5% for a bull (400 kg) during weeks 4 – 6. The during a severe infestation is 27.8 – 41.7% for a cow and 39.3 – 59.0% for a bull during weeks of the energy budget and protein require- ment, are 50 – 70% less than those estimated for calves. These “baseline” estimates for by compounding the costs of pregnant (last trimester) cows and bulls suffering post-rut. Calves are likely the most susceptible to an- nual winter tick-related mortality; however, adults in poor condition may be predisposed to mortality from heavy tick infestations or during tick epizootics, although adults should normally survive during years of average tick abundance. Mortality associated with winter ticks was observed in radio-marked moose in New Hampshire from 2002 to 2005 and was highest in April (75%) corresponding to weeks 4 – 6 of tick engorgement when blood loss was great- est and most concentrated (Musante 2006). ALCES VOL. 43, 2007 MUSANTE ET AL. - METABOLIC IMPACTS OF WINTER TICKS 107 Although tick density was not measured on New Hampshire calves, hair loss and damage was most severe on carcasses in 2002 when calf survival was lowest (0.49) and the highest percentage of tick-related mortality occurred; regional spikes in spring mortality (Samuel and Crichton 2003) and severe coat damage to non-study moose were concurrent. In addition to high and severe levels of infestation and tick-related hair loss/damage, the majority of the calves were emaciated with poor body fat and femur marrow fat ( x = 16.5%) indices, secondary infestations of lungworm, presum- ably Dictyocaulus viviparous, and noticeable paleness of eye mucous membranes, which is a characteristic of anemia in domestic ruminants (Kaplan et al. 2004). Dictyocaulus viviparous is found com- monly in the small bronchioles of lungs in elk calves, and when combined with severe weather conditions, poor host nutrition, or heavy winter tick infestations, has caused morbidity or death of elk (Worley 1979, Thorne et al. 2002). Although D. viviparous is generally not believed related to morbidity of moose (Lankester and Samuel 1998), prevalent infections have been described in calves and yearlings (Pybus 1990). Calf mortalities in Maine during late winter 1995 had infesta- tions of D. viviparous and winter ticks (K. Morris, Maine IF&W, personal communica- tion). While this parasite is probably not the primary cause of death, combined infestations of lungworms and winter ticks may be more detrimental than tick infestations alone. In conclusion, this exercise indicated that blood loss to winter ticks alters protein and energy metabolism of moose calves substan- survival. Our models would underestimate the effects associated with more synchronous and concentrated blood loss. Severely infested calves are more susceptible to late winter mortality; however, the effect of a moderate parasitic infestations, severe winters, and poor body condition. The effect of chronic blood loss is exacerbated by a diet of low quality and digestible protein, and as a result, many calves probably are unable to adequately replace blood and protein loss and become acutely anemic. 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