Comparative response of Rangifer tarandus and other northern ungulates to climatic variability

Robert B. Weladji1*, David R. Klein2, Øystein Holand1 & Atle Mysterud3

'Department of Science, Agricultural University of Norway, P.O. Box 5025, N-1432 Ås, Norway. 2Institute of Arctic Biology, University of Alaska Fairbanks, P.O. Box: 757000, Fairbanks, AK 99775, USA. 3Department of Biology, Division of Zoology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway ""corresponding author ([email protected]).

Abstract: To understand the factors influencing life history traits and population dynamics, attention is increasingly being given to the importance of environmental stochasticity. In this paper, we review and discuss aspects of current knowledge concerning the effect of climatic variation (local and global) on population parameters of northern ungu¬ lates, with special emphasis on reindeer/caribou (Rangifer tarandus). We also restrict ourselves to indirect effects of cli• mate through both forage availability and quality, and insect activity. Various authors have used different weather vari• ables; with sometime opposite trends in resulting life history traits of ungulates, and few studies show consistent effects to the same climatic variables. There is thus little consensus about which weather variables play the most sig¬ nificant role influencing ungulate population parameters. This may be because the effects of weather on ungulate pop¬ ulation dynamics and life history traits are scale dependent and it is difficult to isolate climatic effects from density dependent factors. This confirms the complexity of the relationship between environment and ecosystem. We point out limits of comparability between systems and the difficulty of generalizing about the effect of climate change broadly across northern systems, across species and even within species. Furthermore, insect harassment appears to be a key climate-related factor for the ecology of reindeer/caribou that has been overlooked in the literature of climatic effects on large herbivores. In light of this, there is a need for further studies of long time series in assessing effects of climate variability on reindeer/caribou.

Key words: body mass, caribou, climate change, fecundity, insect harassment, moose, NAO, North Atlantic Oscillation, red , reindeer, sex ratio, survival, weather.

Rangifer, 22 (1): 33-50

Introduction well as identification of the important factors influ• Determining the causes of spatio-temporal varia• encing the traits (Loison et al., 1999a). Most of the tion in life history traits among individuals is one life history traits are influenced by a great number of the main goals of ecology (Begon et al., 1996). of intrinsic and extrinsic interactions that deter¬ This requires long-term studies, accurate estimates mine the developmental process of populations of population sizes and demographic parameters, as (Cappuccino & Price, 1995). In efforts to under-

Rangifer, 22 (1), 2002 33 stand the importance of factors influencing life his¬ Stenseth (1999). Furthermore, we discuss the indi• tory traits and population dynamics of northern rect effect of climate through insect harassment on ungulates, attention is increasingly being given to reindeer/caribou, an aspect that has been largely the importance of environmental stochasticity overlooked by reviews in this field. Indeed, climate (Murdoch, 1994; Turchin, 1995; Putman et al., also acts indirectly on some ungulates, as in the 1996; Sæther, 1997). Density-independent varia¬ case of reindeer and caribou, through interaction tion in phenotypic traits can, if persistent, con¬ with insects that affect their population parameters tribute substantially to population fluctuations in (Anderson et al., 1994; Gunn & Skogland, 1997; ungulates (Sæther, 1997). Some general patterns Mörschel & Klein, 1997; Mörschel, 1999; Colman, have emerged showing, for example, that recruit¬ 2000). A more thorough understanding of these ment is affected more than adult survival (Grubb, mechanisms is made more urgent by global climate 1974; Sæther, 1997; Gaillard et al., 1998). changes that are affecting most northern areas However the effects of weather on population (Hughes, 2000). dynamics in herbivores still remain only superfi¬ cially understood (Sæther, 1997). Climate may act directly on animal behaviour at Climatic variability and plant responses different scales (Helle, 1984; Skogland, 1989; Plant adaptation Kojola, 1991). For example, the direct effect of Because of stochastic variation in climate, plants severe cold or chilling due to rainfall may lead to may develop different survival strategies to cope increased costs of thermoregulation (Parker & with unfavourable environmental conditions. Taiz Robbins, 1985; Putman et al., 1996), and increas¬ & Zeiger (1999) called this «stress tolerance*. At ing snow depth to increased costs of locomotion in northern latitudes, unfavourable and harsh envi¬ snow (Parker et al., 1984). Climate also acts indi¬ ronmental conditions can be persistent (Heide, rectly on ungulate population parameters through 1985), and plant responses to these conditions its effect on plants. Indeed, climatic conditions are include acclimation, as well as adaptation. Because known to have major impact on abundance and of the short growing season and generally low tem¬ nutritional quality of plant tissues available to her¬ perature and variation in photoperiod in the north, bivores (Deinum, 1984; Van Soest, 1994). For some light and temperature are suggested to be the most northern ungulates, much of the variation in popu¬ important factors influencing plant growth and lation parameters has been related to the availabili¬ development (Van Soest, 1994). Because moisture ty of resources in either winter (Skogland, 1985) or stress is an important factor during winter for trees, summer (Reimers et al., 1983; Reimers, 1997; leaf shedding and winter bud formation are impor¬ Hjeljord & Histøl, 1999; Finstad et al., 2000a). tant adaptations (Levitt, 1980). Early leaf develop¬ There have been recent reviews on the effects of ment enables perennial and herbaceous plants to climate on large herbivores (Sæther, 1997) and the utilize short and cool growing seasons, and plants effects of climate in specific geographic areas with adapt to water stress by a limitation in leaf expan¬ either fairly mild (U.K.; Putman et al., 1996) or sion (Taiz & Zeiger, 1999) extreme climates (Gunn & Skogland, 1997; Klein, 1999). However, there has not been a synthesis of Local climatic variation the recent new advances in assessing climatic and forage quality and quantity effects on northern ungulates with an emphasis on Although nutrients, water, light and heat are nec¬ mechanisms, and reindeer in particular. Sæther essary for growth of plants, they have to participate (1997) stressed the need for a better understanding in appropriate proportions for optimal plant of the mechanistic basis behind climatic effects on growth (Jurisson & Raave, 1984). Yearly variation large herbivores. In this paper, we review and dis¬ in forage quality is strongly influenced by weather cuss central aspects of the current knowledge con¬ (B0 & Hjeljord, 1991; Finstad et al., 2000b). cerning the effect of climate (local and global) on Because of the difference in radiation received at population dynamics and life history traits of the soil surface, Bennett & Mathias (1984) found a northern ungulates, with emphasis on reindeer and more than two fold difference in above ground caribou (both Rangifer tarandus). We also consider growth in some plant species as a consequence of recent advances regarding possible mechanisms, slope exposure and associated differences in radia¬ but restrict our focus to indirect effects of climate tion received at the soil surface. Snow cover and mainly on plant quantity and quality, and their depth affect length of the growing season and nutritional importance in the population dynamics hence forage quality (Hjeljord & Hist0l, 1999; Van of northern ungulates as suggested by Post & der Wal et al., 2000). Timing of snowmelt also

34 Rangifer, 22 (1), 2002 influences timing of emergence of forage plants such as reindeer more in contrast to browser, which (Klein, 1985; Langvatn et al., 1996; Post & Klein, could be more flexible. 1999). Most importantly, in years of deep snow there is a prolonged period of access to newly emer¬ Global climatic change gent forage due to a variable time of snow melt. and plant quality and quantity Finstad et al. (2000a) found that annual variations Models of climate change predict that global tem• in summer weather influenced forage availability perature and precipitation will increase within the and digestibility through, for example the varia¬ next century, the changes being more pronounced tion in the Growing Degree Days in May and June. in northern latitudes and during winter Sand et al. (1996) reported that high crude protein (Dickinson, 1986; Maxwell, 1997). Warming levels in birch (Betula sp.) were associated with trends and increased precipitation have been years having low temperatures and high amounts of recorded in many regions of the Arctic during the precipitation in early summer, and high tempera¬ past century, consistent with these climate models tures in late summer. High environmental temper¬ (Chapman & Walsh, 1993; Serreze et al., 1995). atures, however, often lead to increased lignifica¬ Brotton & Wall (1997) also mentioned increased tion of plant cell walls, lowering digestibility. winter snowfall in the Northwest Territories of Amino acids and protein require sugar for their Canada. Both these past and projected climate synthesis, therefore an increased nitrogen supply changes may have affected or may affect the quali• can reduce the sugar content of plant tissues, and ty and quantity of plant material available as forage this effect is promoted at high temperatures and for ungulates through changes they bring about in high light intensity (Deinum, 1984). Cloud cover heat, moisture and available soil nutrients during and shade have been thought to decrease produc¬ the plant growth season (Klein, 1999). In areas of tion of the aboveground plant biomass and the the high Arctic that may experience warmer and nutritive value of forage by affecting the amount of longer plant growth periods with sufficient avail¬ light received by plants (Van Soest, 1994). This able moisture, there will be an increase in plant may be valid where plants require high light inten¬ biomass (Klein, 1999). Post & Stenseth (1999) sity and temperature for optimal growth under found that the North Atlantic Oscillation (a meas¬ short day length at lower latitudes. Restricted light ure of large-scale climatic variability; see below) due to cloud cover and, in the case of forest floor was significantly related to plant phenology, as vegetation, to shade from the crowns of trees, how¬ most plant species bloomed earlier following ever, may improve quality of leaf tissue as forage by increasingly warm, wet winters with herbaceous extending early stages of phenology. This results in species being more sensitive to climatic variation. a low ratio of structural to photosynthesising tis¬ This could have an effect on length of the growing sues and limits accumulation of digestion-inhibit¬ season which, when extended, has the converse ing secondary chemicals derived from carbon that effect of shortening the winter period of plant dor¬ may otherwise be produced in excess of growth mancy (Klein, 1999). This would further lead to needs of plants (Bryant et al., 1983). B0 & Hjeljord increase in winter forage, but with variable quality (1991) found that continental moose ranges (Chapin & Shaver, 1996). The projected increase in improve during cloudy, wet summers. They report¬ cloud cover during summer could result in an ed, after investigation on the most important extension of the period when forage is highly browse species (Betula sp.), that with a decrease in digestible and has relatively low levels of secondary solar radiation, there is an increase in the crude pro- chemicals (Ball et al., 1999; Klein, 1999). This tein:dry matter ratio and a decrease in the tannin could be of great ecological importance at higher content of forage plants. At high latitudes in sum¬ latitudes where the plant growth season is short. mer, the short and cool nights have a positive effect on forage quality because there is little respiratory loss by plants at night (Klein, 1970a) and slow Local climate regime and build up of fibrous tissues. As winter weather varies large herbivore populations annually, snow condition might also vary. Therefore, the availability of forage to ungulates Body weight during winter will be affected. Indeed, cold weath¬ Body weight is one of the most important life his¬ er following wet snow or rain, may lead to ice lay¬ tory traits (Calder, 1984). Several aspects of the life ers in the snow or «icing» on the ground surface history of deer are associated with body weight; limiting access of herbivores to vegetation. This those factors that affect body weight may also have will affect species feeding mainly in the field layers an important influence on population dynamics (Klein, 1970b; Sæther, 1985).

Rangifer, 22 (1), 2002 35 Several studies have shown a relationship body mass of calves and yearling moose with between body weight and conditions on the sum¬ increasing snow depth during the preceding winter mer range (Aarak & Lenvik, 1980; Reimers, 1983; and spring. Furthermore, condition of calves may Langvatn et al., 1996; Sæther et al., 1996; Hjeljord be poor following winters with low temperature & Histøl, 1999). Langvatn et al. (1996) suggest and high snow depth (Sæther & Gravem, 1988; that weight gain of (Cervus elaphus) during Cederlund et al., 1991). Additionally, Cederlund et the early summer growth spurt should be rapid al. (1991) found a negative correlation between during cool May-June weather. They associated body mass loss and snow depth. Snow depth has this with retarded phenological development of been reported to be the only local climatic variable forage plants during periods of cooler weather, that has a significant effect on red deer body mass causing leaf:stem ratios and digestibility of plants in Sør-Trøndelag, Norway (Loison & Langvatn, parts to decline more slowly, thus enhancing qual¬ 1998; Loison et al., 1999b). Similar negative influ¬ ity of the available diet. Climate variables ence was found on black-tailed deer Odocoileus expressed through local weather conditions, there¬ hemionus (Parker et al., 1993), and white-tailed deer fore, can be expected to have a major effect on for¬ O. virginianus (Moen & Severinghaus, 1981). This age quality and quantity in summer, with associat¬ differs, however, from results of studies by Ouellet ed affects on ungulate body size or body weight. et al. (1997) on caribou, as they did not find any Climatic variables, both through their direct effects relationship between winter severity and body con¬ on forage quality and its quantitative availability, dition. can be expected to play a major role in population dynamics of northern ungulates (Table 1). Reproductive performance and sex ratios Sæther (1985) found that a combination of Age at maturity and fecundity are strongly related many climatic variables explained a significant por¬ to body weight and condition (Lenvik et al., 1988; tion of annual variation in mean carcass weight of Gaillard et al., 1992; Jorgenson et al., 1993; Festa- moose (Alces alces) in autumn. Mean summer tem¬ Bianchet et al., 1994; Langvatn et al., 1996; Sæther perature and summer precipitation were the most et al., 1996; Reimers, 1997). Therefore, climatic important variables. Sand et al. (1996) reported variation is expected to affect these life history that years with relatively high body mass of moose parameters (Table 1), but this relationship may, in Sweden were generally associated with low tem¬ however, differ regionally due to different selective perature and high amounts of precipitation in early regimes (Sæther et al., 1996). summer, and with high temperatures and low pre¬ Finstad et al. (2000b) reported that the propor¬ cipitation in late summer and early fall. They also tion of reindeer yearlings lactating in June was pos¬ found a positive correlation, although significant itively related to Growing Degree Days the previ¬ only for adult females, between previous winter ous May and June and negatively related to both snow and body mass, suggesting a delayed effect of Growing Degree Days the previous July and snow weather variables on body mass. depth the winter prior to birth. Cameron et al. The effects of winter climate appear also to be (1993), reported that the probability of a successful important, through, for example, the indirect effect pregnancy of female caribou may be largely prede¬ of late snow melt on forage quality or snow condi¬ termined during the previous breeding season, tion on forage availability, but direct effects may based on autumn condition, whereas maternal con¬ also be important. In years with high snowfall, dition during late pregnancy has greatest influence caribou calves were lighter at 10 months of age and on calving date and early calf survival. Sand et al. presumably unable to gain sufficient mass by (1996) found in Sweden that high fecundity and autumn to breed successfully as yearlings (Adams recruitment rate of moose were associated with & Dale, 1998). Negative correlations between body years having relatively warm September weather. mass and severity of the preceding winter have The proportion of 2-year-old red deer calving in been reported for wild reindeer (Skogland, 1983). Norway, and cohort differences in the proportion Gerhart et al. (1996) associated winter undernutri- calving as 3-year-old red deer on Rum, Scotland, tion with declines in body fat and protein in adult were negatively related to variation in May-June female caribou. This was not the case on degree days 12 months earlier (Langvatn et al., Southampton Island, Canada, where caribou condi¬ 1996). They also revealed that the proportion of tion (measured as bone, muscle and empty body hinds calving on Rum had a tendency to decline mass) did not appear to be related to the winter with increasing number of days with snow in win¬ severity index (Ouellet et al., 1997). Hjeljord & ter. Winter conditions, thus also influence repro¬ Histøl (1999) also reported a decrease in autumn duction. The reproductive performance of female

36 Rangifer, 22 (1), 2002 caribou (2, 3, 4 and 6 year olds) was affected by 1991). Annual variation in population growth rate winter snowfall with natality declining with in Svalbard reindeer was strongly negatively relat¬ increasing late winter snow fall during the winter ed to winter precipitation. High growth rate prior to the autumn breeding season (Adams & occurred when winters were dry, and the effect of Dale, 1998). In Southern Norway Sæther et al. climate was stronger at high densities (Aanes et al., (1996) found that female moose also matured earli¬ 2000). Survival rates of red deer calves of both sexes er after two winters with almost no snow cover. were positively correlated with temperature and Similarly, delayed maturity was found on mountain negatively with snowfall, while only a slight nega¬ goats (Oreamnos americanus) in a population livingtiv e effect of day-degrees on yearling survival rate under harsh winter conditions (Jorgenson et al., was detected in males and a slight positive effect of 1993). Kruuk et al. (1999) found that fecundity of day-degree was detected on adult male survival female red deer decreased with rainfall in the pre¬ rates (Loison & Langvatn, 1998). A negative effect ceding winter. of winter harshness was found for red deer on Rum, Recently, climate variables have been demon¬ Scotland (Clutton-Brock & Albon, 1982), with a strated to affect population sex ratios in red deer lower male than female survival rate (Table 1). (Kruuk et al., 1999; Post et al., 1999b; Mysterud et Juvenile mortality was observed to increase during al., 2000). The proportion of male red deer born winter with both high population density and high yearly on the island of Rum, Scotland, declined November-January rainfall (Kruuk et al., 1999). with winter rainfall, associated with increased Studies by Jorgenson et al. (1997) in bighorn sheep nutritional stress in females (Kruuk et al., 1999). In (Ovis canadensis), and Loison & Langvatn (1998) did Norway, the proportion of male red deer harvested not detect a relationship between winter severity during autumn each year declined with increasing and adult survival. These observations show that snow depth in March (Mysterud et al., 2000). The there are differences in mortality by sex and age annual sex-ratio was not related to e.g. sex-depend¬ class within a population in response to weather ent mortality during the summer season. Female variables. In wapiti (Cervus canadensis), calf survival red deer thus reared fewer sons as nutritional stress rate correlated positively with July temperature increased with increasing severity of climate both and negatively with November precipitation while on Rum, Scotland and in Norway. The extrinsic cow survival was positively correlated with January modification of ungulate sex ratios by climate temperature, but negatively correlated with May occurs at a population scale and is probably not temperature and total July precipitation (Sauer & Boyce, 1983). It is noteworthy that, the effect of adaptive (Kruuk et al., 1999; Post et al., 1999b; climate interacts with population density. Indeed, Mysterud et al., 2000). However, the physiological the effect of winter weather on survival of wapiti mechanism by which sex ratio is determined cows and calves seemed stronger at high population remains unknown (Hewison & Gaillard, 1999). density (Sauer & Boyce, 1983). Possible mechanisms include a higher in utero mor¬ tality of males under harsh conditions, and modifi¬ Mortality is sometimes also attributed to sum¬ cation of the sex ratio at conception and/or implan¬ mer conditions. Comparing latitudinal gradient tation (Reimers, 1999; Mysterud et al., 2000). both in summer and winter range condition in dif¬ ferent Norwegian moose populations, Sæther et al. Survival, abundance and population growth (1996) found that mortality was highest in the A close relationship has been reported between northernmost study area, where most death winter weather and both annual mortality rate in occurred during summer and very few calves died several species of ungulates (Martinka, 1967; during winter. They found no relationship between Clutton-Brock & Albon, 1982; Sauer & Boyce, winter food supply and calf mortality. Stubsjøen et 1983; Skogland, 1985; Gaillard et al., 1993;) and al. (2000) found seasonal variation in survival abundance of calves (Lee et al., 2000). Direct effects among calves but very little among adults, in three of winter climatic conditions on survival are com¬ populations of moose in northern Norway. The monly reported, but there may also be effects of highest mortality was found among neonates dur¬ summer weather. ing summer in two populations. The natural mor¬ Skogland (1985), comparing different wild rein¬ tality of calves was different among regions during deer herds, revealed a relationship between calf sur¬ both summer and winter. Stubsjøen et al. (2000) vival rate and the amount of forage available during attributed part of the natural mortality to severe late winter. Caribou in northwestern Alaska also climatic conditions in both winter and summer. experienced highest calf mortality in years when Early survival in roe deer (Capreolus capreolus) fawns snowmelt was relatively late (Fancy & Whitten, tended to increase with increasing rainfall in May

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The cohort survival malian herbivores, including phenotypic variation, of the chamois (Rupicapra rupicapra) has been fecundity, sex ratios, demographic trends and pop¬ reported to increase when precipitation was high ulation dynamic processes (Post et al., 1997, and temperatures were low during the preceding 1999a,b,c; Forchhammer et al., 1998; Post & spring in the Pyrenees, while no cohort effect was Stenseth, 1998, 1999; Loison et al., 1999a; detected in the Alps, but decreased survival Mysterud et al., 2000). Global climate change will occurred following a low degree-day spring (Loison likely increase both the extent and seasonal dura¬ et al., 1999a). In an investigation of the regional tion of open water in the arctic seas, and the fre¬ effect of climate on reindeer, Lee et al. (2000) found quency of oceanic cyclonic storms at high latitudes that the number of live calves recorded in northern (Serreze et al., 1995). Icing events can, therefore, be Finland was negatively related to both warmer and expected to increase, limiting access to forage by wetter winter weather prior to the rut, and posi¬ caribou (Klein, 1999). Such broad patterns of glob¬ tively to warmer autumn weather prior to birth al change will affect most herbivore population (Table 1). This study did not specify when live calf parameters (See Gunn & Skogland, 1997; Table 2). numbers were recorded and did not include snow characteristics in their models. Body mass, fecundity and sex ratios There is a correlation between the NAO and red deer cohort-specific mean body weight and skeletal Global climatic regime ratios of adults when cohorts were in utero (Post et and large herbivore populations al., 1997). Recently, however, opposite correlations In the North Atlantic region, winter climatic vari¬ between the NAO and red deer body weight were ability is, to a large extent, explained by a large- reported from the same area in Norway; both high scale alternation of atmospheric pressure called the body weights of red deer calves (Loison et al., North Atlantic Oscillation (NAO) (Rogers, 1984; 1999b) and low body weights of adult red deer Hurrell, 1995). The NAO refers to a meridional (Post et al., 1997) followed years with positive oscillation in atmospheric mass with centres of NAO. Mysterud et al. (2000) found that the con¬ action near Iceland and over the subtropical trasting result was because Post et al. (1997) did Atlantic from the Azores across the Iberian not control for the stronger and negative effect of Peninsula (Hurrell, 1995). Because the signature of local density, as both density and the NAO the NAO is strongly regional, its state is quantified increased during the span of the study. A high annually by a simple index based on the mean devi¬ NAO index was indicative of higher precipitation. ation from the average sea-surface pressure between As winter temperatures at the west coast of Norway the Azores and Iceland, from December through is commonly around 0 °C, the warmer tempera• March for the winter. Positive values of the NAO- tures, however, at higher NAO (Hurrell 1995; Post index characterize unusually warm, wet winters in et al., 1997) result in a negative correlation northern Europe (and unusually cold, dry winters between snow depth and the NAO at low eleva¬ in North America), while negative values charac¬ tion, whereas this relationship is reversed above terize unusually cold, dry winters in northern approximately 400 m a.s.l. (Mysterud et al., 2000). Europe (and warm, wet winters in North America) Forage in the field layer is thus probably more eas¬ (Hurrell, 1995). Because the NAO accounts for ily available to red deer in these coastal and low¬ most of the year to year fluctuations in winter pre¬ land areas during winters with a high NAO index cipitation in northern latitudes (Hurrell, 1995, (Loison et al., 1999b), and a high NAO index thus 1996; Hurrell & Van Loon, 1997) as well as varia¬ probably indicates favourable conditions for red tions in wintertime temperatures on the scale pre¬ deer. Indeed, body weights of red deer in Norway dicted by theoretical models of climate change in general were positively correlated with the NAO (Hurrell, 1996), the NAO has a clear potential to when taking population substructure into account affect the ecology of plants and in the and using an index for local density, although this Northern Hemisphere (Post et al., 1999a). relationship was reversed at very low NAO values However, as the effect of this large-scale climatic (A. Mysterud, N.G. Yoccoz, N.C. Stenseth & R. index may result in different local weather patterns Langvatn, unpublished results). in different areas (Mysterud et al., 2000), these On Rum, Scotland, Post & Stenseth, (1999) interactions are inherently complex. observed that birth mass and adult mass of red deer The NAO, through its effects on vegetation and increased following positive (warm, wet) NAO climatic conditions, influences several aspects of winters while fecundity of female red deer correlat¬ life history and ecology of terrestrial large mam- ed negatively with the NAO index of the winter in

40 Rangifer, 22 (1), 2002 which they were in utero. They also reported a neg¬ temperature and low precipitation in winter) ative relationship of both reindeer calf mass and exhibited low winter survival in the Pyrenees, female fecundity with NAO in Finland and while in the Alps, survival decreased following pos¬ Norway respectively (Table 2). On the contrary, itive NAO. Accordingly, they suggested that com¬ Loison et al. (1999b) found that body mass of red mon ideas about effect of winter harshness and deer was positively correlated to NAO, but lagged snow on survival of herbivores are more complicat¬ one year. Also, while yearling moose in Norway ed than assumed previously. were heavier if born following positive NAO win¬ On the western side of the Atlantic, caribou, ters, body mass of moose in Sweden, where winter moose, muskox (Ovibos moschatus) and white-tailed weather was more continental, declined following deer abundance increased following high NAO warm, wet winters (Post & Stenseth, 1999). This (Table 2) in West Greenland, Isle Royale, East suggests that the effect of NAO on population Greenland and Minnesota respectively (Post & parameters varies regionally. Post et al. (1999c) Stenseth, 1999). The rates of increase of both documented recently that the state of the NAO moose and white-tailed deer in North America during fetal development of hinds in red deer influ¬ were influenced by global climatic fluctuation at 2 enced the mass of their sons, but not daughters. and 3 years lags, as well as delayed density-depend¬ Winters with a high NAO index also led to ence feedback and wolf predation (Post & Stenseth, increasingly male biased sex ratios of offspring, 1998). independent of changes in the mean age of hinds (Post et al., 1999b; Mysterud et al., 2000; Table 2; see also discussion above). There was, however, no Climate, insect activity and harassment residual effect of the NAO once the effect of snow Studies discussing effects of climatic variability on depth (at low elevation) was controlled for male- ungulate populations have generally not related it biased harvest with increasing snow depth to the effects of insects. However, this mechanism (Mysterud et al., 2000). may potentially be very important. Klein (1991) suggested that harassment by the skin warble Abundance and survival (Hypoderma tarandi, Oestridae) and nasal bot flies In red deer, Forchhammer et al. (1998) observed (Cephenemyia trompe, Oestridae), introduced to that, warm, moist winters (high NAO) were asso¬ Greenland in the 1950s, and infestation by their ciated with decreased abundance (through over¬ larvae may have been a major factor influencing winter mortality the following year), whereas the decline in body condition and suppression of the delayed two-year effect of warm, moist winters had population of West Greenland caribou. a positive effect on abundance (through increased Syroechkovskii (1995) estimated that caribou or fecundity of the cohort born following high NAO), reindeer could lose up to 2 kg of blood to mosqui¬ with the positive effects being relatively larger. toes during one season in the Taimyr Peninsula, They suggested that the NAO effect was sex-spe¬ Russia. Colman (2000) reported lower body mass cific, operating primarily through the female seg¬ in the southernmost population of reindeer in ment of populations. It also has been shown that Norway after a summer with severe insect harass¬ male and female calves responded differently to cli¬ ment than after a cool summer (Table 3). It has matic variability (Post et al., 1999c). Post et al. appeared in the same area and during the same (1999a) reported that in both S0r-Tr0ndelag period that free ranging sheep weight was higher in (Norway) and Rum (Scotland), total abundance of the year with warmer summer (unpubl. data), sug¬ red deer increased two years after increasingly gesting that the pasture was not of bad quality, and warm winters (Table 2). Whereas in Norway, this that insect harassment may affect reindeer/caribou increase was attributed to the enhancement of body condition independently of range quality. cohort specific fecundity of 2 year-old hinds, on Considerable behavioural evidence supports harass¬ Rum it was attributable to increases in annual ment by insects as the most important causal link fecundity of 3 year-old hinds. Indeed, adult male between warm summer temperatures and low body abundance was negatively correlated to the previ¬ condition of reindeer. Indeed, dense aggregations ous NAO on Rum (Post & Stenseth, 1999). Both and associated movement of reindeer and caribou abundance (Post & Stenseth, 1999) and lamb sur¬ during warm summer weather are associated with vival (Milner et al., 1999) of Soay sheep (Ovis aries) insect harassment (Anderson & Nilssen, 1996; have also been reported to decrease following high Noel et al., 1998), which results in increased time NAO. Loison et al. (1999a) found that adult cham¬ spent moving and/or standing, and reduced time ois born after positive NAO (indicative of high spent feeding, with detrimental nutritional conse-

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s u ss el o o r i gg g gg b la ia ter vi i aa ar aa u e l v r ar ar s s ar ee rs rs ic in p e a a yy y at nar ee OOOOOOOOO O OOO O vioO yy li m v ee AAAAAAAAA AAAAA re A 3 2 Cl h y NNNNNNNNN NNNNN PrN O O s) AA w 1 d NN in s OO e ee r AA c hi te s s NN ) aa t n el > e al ee d m o rr m a ty 't cc ana e m inin nd f al l ar nc o f f a c a u x v oo i p e a e n v c b cc v h c a r c c s s p i m n lu ei nd el so ln ana a ce v ap pi g a l aa s tete r y li n ti n r t t y n d v dd gt u 6 r v t an u a a l n iv lnn d s rr oo ar u lu l r uuu d ab u mo r n b n b t u dbb me e o d um Y um p u A TA t o S AAA bu am ee A L ur Deph u Pr p r r A ( s e s e e x e e oi ei d o h te ci d sk in ^ïevv e s d m s her ei o s p o e a S R h u ay e Mo R C o Wd Mu S 42 Rangifer, 22 (1), 2002 quences (Helle et al., 1992; Toupin et 6 9 77 al., 1996; Mörschel & Klein, 1997; 9 99 99 Colman, 2000). Using activity n, change per minute as an indicator of e 6, , 6 s 2 9inin 9 harassment, Mörschel & Klein s 9 9eiei 9 i 90 N 0 1 0 0 . (1997) reported higher rate of activ• , l 0 . 0 al & & a ity changes among caribou in central •a 2 l. e a 2 et c n, , et el Alaska when insects were present. c s n u a n n h d l a i sc e e r Temperature and wind speed had a r p s lla e -a lm el m r f l uö o o o significant effect on the rate of activ¬ e ol l < H CooTM ity changes of caribou (Table 3), R C P reflecting the regulation of insect activity by these abiotic factors. Behavioural responses to avoid y wa insects are commonly observed. or Indeed, as reported by Pollard et al. A AA A N (1996), caribou movements, distri¬ S n SS S ty y, r d ya , S , S , a bution, and behaviour were signifi¬ aaUS e n ana U Ua , al rwsk th a wadkk ut ks cantly influenced by harassment r s l r n as as c o a la o o in o a l l Al from parasitic insects such as mos¬ L NoAl S quitoes and oestrids, during the post-calving period. Espmark & Langvatn (1979) reported that lying down was a strategy to cope with

g e head fly harassment in red deer in in ng Norway. This indicates a possible d g as a in e h detrimental effect of insect harass¬ e vicre c ment also on other species of deer. aj oe ty > i c iv m d t Three major parasitic insects are n a d tt d c en n n of primary concern for reindeer: mos• o a fo ea quitoes (especially Aedes sp., s n e oi Culicidae), warbles flies and nasal c at r n g bot flies (Gunn & Skogland, 1997; e re e u g Mörschel & Klein, 1997). But, q g s ea Anderson & Nilssen (1998) reported e A cr s evidence for potential contribution In ns to the harassment on reindeer by o c ecece black flies (Simuliidae) and horse cncnc d naa and deer flies (Tabanidae) as well. a te d dd t n nn la Roby (1978) observed a higher per¬ unbubu re centage of standing and running and d ababab n o o a nt to it it a lower percentage of lying under it i i u u u t e u y q qq oestrid fly harassment than under bil ia m i qss similar levels of mosquito harass¬ ar s 2 0 0 ment. Mörschel & Klein (1997) v dee e o o o as e eese m m m ic a e e ar a es s as found that the presence of oestrid a s aaea ess t e a h re r ee flies had a larger influence on activi¬ lim eere ass a c rerr c e c cc ct n I ee l aeea ty budgets of caribou than did mos¬ c e rrcr Q e e s er r quitoes by substantially increasing to In s ty ty e s rcc i i the amount of time spent standing s r r r id yid cecec ns el e e e and decreasing the amount of time b e r m e it m o ia e r de u dr c u i m mr rm ur ed e u ed ur oc u spent feeding. p a r r er t e v h e t l h .0 m mtu v m a o ae 0. s pc e p e v t v rs c es rv e It is during summer, which is the e u ua o u e iv e iv r ic V e p d ud ati d p d ati peak period in energy and nutrient ct at m m p ud m m in o el in m in el e lim intake and requirement for northern s In 3. Cl Rangifer, 22 (1), 2002 el 43 ablT ungulates that harassment by insects occurs. plant quantity might be driven by low levels of Russell (1993) reported that the warble and nasal available plant biomass and high forage quality bot fly season lasted from the end of June until during the growing season in the high arctic, early August, while mosquitoes were primarily a whereas in temperate regions with high forage bio¬ problem in July. In Norway the oestrid season lasts mass, selection for plant quality may be of greater from 10 July and ends around 20 August (Nilssen importance for herbivores. In Svalbard reindeer, & Haugerud, 1994). Although there is consider¬ therefore, selection for high plant biomass is likely able range in how the combination of weather vari¬ to lead to a more favourable nitrogen and energy ables affect levels of insect harassment, it is clear return than selection for high plant quality (Van that temperature, wind and relative humidity are der Wal et al., 2000). the primary interacting factors for reindeer and Although the existence of effects of weather caribou, the relative importance of each varying parameters (local and global) on ungulate popula¬ with terrain features, location (altitude and lati¬ tion dynamics is widely accepted, there is little tude), vegetation and substrate type, and animal consensus on the direction (positive or negative) of group size and behaviour. Walsh et al. (1992) used its effects and on which variables are more impor¬ an ambient temperature «greater-than-or-equal- tant. Some of the contrasting results probably arise to» 13 °C and winds «less-than» 6 m/s to predict from methodological differences, or failure to insect harassment while Brotton & Wall (1997) account for other significant covariates, such as suggested a minimum temperature of 6 °C for density (see e.g. Mysterud et al., 2000 and discus¬ oestrid fly activity. But, although he hypothesized sion above). For example, Mech et al. (1987) docu¬ that summer climate was responsible for differences mented the cumulative negative effects of previous observed among years in larval infestation levels, winters' snow on rates of population increase in Nilssen (1997) has shown that cold weather certain moose and white-tailed deer. Messier (1991) years may affect oestrids populations very strongly. analysing a smoothed version of the same dataset Pollard et al. (1996) found that mosquito abun¬ reported no effect of snow accumulation on popula¬ dance was positively correlated with temperature tion dynamics. Post & Stenseth (1998) reanalysed and negatively correlated with wind velocity and both original and smoothed data on dynamics of relative humidity in Alaska. Colman (2000) report¬ moose and white-tailed deer accounting for serial ed insect harassment of wild reindeer in southern autocorrelation and using the NAO (which has a Norway to be positively correlated to increasing correlation with snowfall) and found that rates of temperature and negatively correlated with increas¬ increase of moose and white-tailed deer in both ing cloud cover (Table 3). original and smoothed data were influenced by global climatic fluctuation at 2- and 3-year lags. However, Loison et al. (1999a) reported opposite Discussion effects of increase in spring temperature on cham¬ ois in the Alps and Pyrenees, showing different Several studies have been carried out investigating local response to the same global climatic variabil¬ the influence of local and global weather variation ity at the intra-specific level using the same on plants, and how this in turn affects population methodology. This suggests that contrasting parameters of northern ungulates (Table 1). The responses to climate cannot be all explained by indirect effect of climate through its impact on methodological problems. There is considerable vegetation is confirmed through field studies show¬ biological variation in response to climate between ing that increased solar radiation and temperature regions, areas, and localities, between species and lead to increased levels of secondary compounds in even within species. plant tissues, such as phenols and tannins, while lowering the crude protein:dry matter ratio of tem• Also, most studies using the NAO have not perate forage plants (Jonasson et al., 1986; Laine & clearly shown its relationship with local weather Henttonen, 1987; B0 & Hjeljord, 1991). The inte¬ variables of the sites actually studied. There is evi¬ grated effects on availability of food resources per dently little consensus among authors on the gen¬ capita, on environmental conditions and on previ¬ eralized relative importance of specific climatic ous reproductive success determine productivity of variables in influencing ungulates population ungulates. Therefore, environmental conditions parameters. There is considerable regional and local such as adverse weather can be a significant influ¬ variability in how ungulates respond to specific cli¬ ence even for highly productive ungulates occur¬ matic variables (Klein, 1999). This demonstrates ring at low densities (Adams & Dale, 1998). Van the complexity of the environmental/ecosystem der Wal et al. (2000) suggested that selection for relationships that also vary regionally, locally and

44 Rangifer, 22 (1), 2002 by species and population status (sex, age and size of the adult phase of these Dipteran species, their for example). This suggests that we should ques¬ life span and their activity and flight capacities tion the factors guiding choices of some specific under different temperature, humidity and wind weather variables and not others by authors in this conditions (see Roby, 1978; Russel, 1993; field, as statistically it is often possible to find cor¬ Mörschel & Klein, 1997 above). Summer weather, relations among variables after several trials (e.g. through its effects on insect activity may play a Lindström, 1996). detrimental role on reindeer/caribou condition dur• ing summer, temperature being a key factor. Indeed, various means have been used to investi¬ A reindeer/caribou perspective gate and evaluate the effect of insects on reindeer In view of their numbers and, their socio-cultural and caribou, and temperature has consistently and economical importance, there is a need for appeared to play an important role in determining studies of long time series in assessing effects of cli¬ the level and type of avoidance behaviour of rein¬ matic variability on reindeer/caribou. Indeed, many deer and caribou, even in the immediate absence of northern indigenous peoples, including the insects (Mörschel & Klein, 1997). The expected Gwich'in of Alaska and northwestern Canada, the increased temperature with ongoing global climate Inuit of Canada, Alaska and Greenland, the Sami change could, therefore, be more harmful for rein¬ and Komi of Fennoscandia and western Russia, and deer than other northern ungulates. We thus point numerous other peoples of Siberia and the Russian out the limits of comparability between systems Far East have dependence on reindeer/caribou for and the difficulty of generalizing about the effect of their livelihood. Reindeer areas in Norway experi¬ climate change broadly across northern systems, ence large annual climatic variations with severe across species and even within species. The project¬ impacts on herd reproductive output, as both live ed increased temperature in Scandinavia and other and dressed weight for calves and adults vary year¬ parts of the Eurasian and American North could ly in connection with climatic variation therefore lead to increased detrimental effects on (Reindriftsforvaltningen, 1998; R.B. Weladji & 0. reindeer and caribou through its effect on insect Holand, unpubl. results). Furthermore, probably to activity when temperature, wind velocity and rela¬ a much greater degree than other ungulates, insect tive humidity are appropriate. The complex role of harassment and associated parasitism, which is insects in the ecology of reindeer and caribou, and related to summer weather conditions, is of partic¬ the associated influence of weather parameters on ular importance in their ecology (Mörschel & the ecology of these insects, renders assessment of Klein, 1997; Klein, 1999; Colman, 2000). The climate variability on the population dynamics of total foraging time is considered to be a main reindeer and caribou particularly difficult. Even determinant of fattening in Rangifer (Reimers, less is known regarding possible effects of other 1980). It is apparent that insect harassment during parasitic groups. Halvorsen et al. (1999) reported warm summers can have a detrimental effect on evidence for transmission of parasitic nematodes in body condition and productivity of reindeer and Svalbard reindeer during the arctic winter. caribou through lost foraging time, increased ener¬ Accordingly, as global changes are predicted to gy expenditure and increased parasite burden. affect winter climate the most, parasitic survival Models investigating the effect of climate change and transmission may increase with increased win¬ on reindeer predict an increase in insect harassment ter temperature. The relationship between climate in summer, due to an increase in average monthly and parasites in general should therefore be further temperature (Gunn & Skogland, 1997; Brotton & evaluated. Wall, 1997). This may vary locally, however, because the level of harassment may vary depend¬ The affiliation between reindeer/caribou and ing on wind velocity, as insect harassment is lichen is very strong (Boertje, 1990; Crittenden, reduced on windswept areas (Walsh et al., 1992). 2000). Precipitation is one of the major processes Other factors influencing insect levels and their that deliver nutrients to lichens (Crittenden, harassment include cloud cover (Colman, 2000), 2000). Thus, increased precipitation during win¬ relative humidity and access to «insect relief» habi• ters as predicted by climate change models tat (Pollard et al., 1996; Mörschel & Klein, 1997). (Dickinson, 1986; Maxwell, 1997), may lead to The effects of mosquitoes, biting flies, warble flies improved reindeer/caribou ranges during winters. and nasal bot flies on reindeer and caribou may vary But in the presence of other plant types and under differentially in relation to weather conditions. improved winter conditions, the competition edge This is related to the different timing of emergence of lichens may be reduced, leading to lichens shrinkage and to reduction of the mat-forming

Rangifer, 22 (1), 2002 45 lichens, which might be detrimental for reindeer Skjelvag, A.O. (eds.). The impact of climate on grass pro• and caribou. duction and quality. Proceedings of the 10th General Predictions about possible effects of the ongoing Meeting of the European Grassland Federation. As, global warming cannot be made with certainty, but Norway, 26-30th June, pp. 90-94. they will most likely be detectable, although vari¬ Bø, S. & Hjeljord, O. 1991. Do continental moose able between different geographic areas. range improve during cloudy summers? — Can. J. Zool. 69: 1875-1879. Boertje, R. D. 1990. Diet quality and intake require¬ Acknowledgment ments of adult female caribou of the Denali herd, We gratefully acknowledge the financial support of the Alaska. — Journal of Applied Ecology 27: 420-434. Norwegian Reindeer Husbandry Development Fund to Brotton, J. & Wall, G. 1997. Climate change and the R.B. Weladji and Ø. Holand. The authors express grati• Bathurst Caribou herd in the Northwest Territories, tude towards the Circumpolar PhD Network in Arctic Canada. — Climatic Change 35: 35-52. Environmental Studies who allowed R.B. Weladji to par• Bryant, J. P., Chapin, F. S., III & Klein, D. R. 1983. ticipate in their course «Reindeer as a Keystone Species Carbon/nutrient balance of boreal plants in relation to in the North» in September 2000, where this work was vertebrate herbivory. — Oikos 40: 357-368. discussed in a seminar session. We are also grateful to the Calder, W. A. 1984. Size, function, and life history. anonymous reviewers and to O. Hjeljord for making sug¬ Harvard University Press, Cambridge, Massachusetts gestions that improved the manuscript. and London, England. Cameron, R. D., Smith, W. T., Fancy, S. G., Gerhart, K. L. & White, R. G. 1993. Calving success of References female caribou in relation to body-weight. — Can. J. Aanes, R., Sæther, B. E. & Øritsland, N. A. 2000. Zool. 71: 480-486. Fluctuations of an introduced population of Svalbard Cappuccino, N. & Price, P. W. 1995. Population dynam• reindeer: the effects of density dependence and cli• ics, new approaches and synthesis. London: Academic matic variation. — Ecography 23: 437-443. Press. Aarak, E. & Lenvik, D. 1980. Weight development in Cederlund, G. N., Sand, H. G. & Pehrson, A. 1991. young reindeer. — In: Reimers, E., Gaare, E., & Body mass dynamics of moose calves in relation to Skjenneberg, S. (eds.). Proceedings 2nd Int. Reindeer winter severity. — J. Wildl. Manage. 55: 675-681. Caribou Symp. Røros, Norway, 1979. Direktoratet for Chapin, F. S., III & Shaver, G. R. 1996. Physiological vilt og ferskvannsfisk, Trondheim, pp. 355-359. and growth responses of arctic plants to a field of Adams, L. G. & Dale, B. W. 1998. Reproductive per• experiment simulating climatic change. — Ecology 77: formance of female Alaskan Caribou. — J. Wildl. 822-840. Manage. 62: 1184-1195. Chapman, W. L. & Walsh, J. E. 1993. Recent variations Anderson, J. R. & Nilssen, A. C. 1996. Trapping of sea ice and air-temperature in high-latitudes. — oestrid parasites of reindeer: The response of Bulletin of the American Meteorological Society 74: 33-47. Cephenemyia trompe and Hypoderma tarandi to baiteClutton-Brockd , T. H. & Albon, S. D. 1982. Winter traps. — Medical and Veterinary Entomology 10: 337¬ mortality in red deer (Cervus elaphus). — J. Zool. London 346. 198: 515-519. Anderson, J. R. & Nilssen, A. C. 1998. Do reindeer Colman, J. E. 2000. Behaviour patterns of wild reindeer in aggregate on snow patches to reduce harassment by relation to sheep and parasitic flies. PhD thesis. parasitic flies or to thermoregulate? — Rangifer 18: 3¬ University of Oslo, Oslo, Norway. 17. Crittenden, P. D. 2000. Aspects of the ecology of mat- Anderson, J. R., Nilssen, A. C. & Folstad, I. 1994. forming lichens. — Rangifer 20: 127-139. Mating behaviour and thermoregulation of the rein• Deinum, B. 1984. Chemical composition and nutritive deer warble fly, Hypoderma tarandi L. (Diptera: value of herbage in relation to climate. — In: Riley, H Oestridae). — Journal of Insect Behaviour 7: 679-706. & Skjelvag, A.O. (eds.). The impact of climate on grass Ball, J. P., Ericsson, G. & Wallin, K. 1999. Climate production and quality. Proceedings of the 10th General changes, moose and their human predators. - Meeting of the European Grassland Federation. As, Ecological Bulletins 47: 178-187. Norway, 26-30th June, pp. 338-350. Begon, M., Harper, J. L. & Townsend, C. R. 1996. Dickinson, R. 1986. The climate system and modelling Ecology. 3rd ed. Blackwell Science. of future climate. — In: Bolin, B., Doos, B., Jager, J. & Bennett, O. L. & Mathias, E. L. 1984. Effects of slope Warrick, R.A. (eds.). The greenhouse effect, climate and microclimate on yield and forage quality of change, and ecosystems. Wiley, Chichester, UK, pp. 207¬ perennial grasses and legumes. — In: Riley, H. & 270.

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