As in other seasonal environments, herbivores in the Arctic display seasonal reproduction which is timed to coincide with a highly pulsed peak in resource availability (Post 2003a). Caribou and wild reindeer (both Rangifer tarandus), for instance, exhibit highly synchronous parturition that coincides with the onset of the plant-growing season (Skogland 1989; Post & Klein 1999; Post et al. 2003). However, both the timing and duration of the plant-growing season are expected to respond to climate change in the Arctic (Molau 1997), with the onset beginning earlier and the duration possibly shortening as abiotic constraints on phenological progression are alleviated (Post et al. 2001, in press). Indeed, numerous studies have already documented shifts in the timing of plant growth at high latitudes associated with recent climate change (Walther et al. 2002; Post 2003b; Forchhammer et al. 2005). There is, therefore, potential for development of a trophic mismatch between the timing of caribou arrival on their calving ranges and the timing of peak resource availability on-site. Such a trophic mismatch could have negative consequences for offspring production and survival in mammalian herbivores such as caribou because the energetic demands of lactation, which would otherwise be met by intake of newly emergent plant tissue at peak nutritional value, are the highest resource demands of the annual reproductive cycle (Robbins 1983; Clutton-Brock 1991).

Numerous recent studies have focused on adverse effects of recent climate change on caribou populations throughout the Arctic. In the High Arctic of Canada, a population of the endangered Peary caribou (Rangifer tarandus pearyi) recently experienced a catastrophic and near-total population crash associated with increasing winter snow and ice crust formation consistent with climate change projections (Miller & Gunn 2003). As well, the dynamics of multiple populations of caribou in West Greenland have become synchronized towards the end of the twentieth century in response to rising winter temperatures (Post & Forchhammer 2004). Furthermore, dynamics of caribou and reindeer populations throughout the Northern Hemisphere respond to fluctuations in the North Atlantic Oscillation/Arctic Oscillation (Forchhammer et al. 2002; Post 2005), and in some cases are entrained to the point of highly synchronous dynamics across distances of thousands of kilometres (Post & Forchhammer 2006). Such climate-induced synchrony represents a potentially adverse consequence of climate change because synchronously fluctuating populations face a greater risk of global extinction than do independently fluctuating populations (Palmquist & Lundberg 1998).

Among years, the timing of onset of the plant-growing season was most closely related to mean April temperature (r=−0.57; p=0.20). Timing of onset of caribou calving displayed its strongest correlation to mean spring (March–May) temperature (r=−0.71; p=0.12). Onset of calving was not, however, closely correlated with that of the plant-growing season (r=0.04; p>0.50), presumably because, as noted above, the onset of plant growth was considerably more variable among years than was the onset of calving (figure 1). Mean spring temperature, over the course of the study, increased by 4.63°C, though the correlation with ‘year’ is only marginally significant (r=0.52, p=0.058). We assume that the poor correlation of onset of the growing season with any of our abiotic predictors may be explained by either or both of the following factors. First, because our sampling did not begin early enough to record observations of 0 species emergent (figure 1a), our nonlinear regression estimates of the beginning of the growing season each year are less precise than those of the onset of calving (figure 1b). Second, as in other parts of the Arctic, onset of the plant-growing season may be determined by the combined influences of temperature and snow cover (Høye et al. 2007), and our sample was too small to justify multiple regression analysis.

The progression of the plant-growing season was closely related to its onset, as the date of emergence of 50% of forage species was highly positively correlated with the date of emergence of 5% of species (r=0.84, p<0.05). Hence, warm springs were followed by early onset and rapid progression of the plant-growing season. In turn, a more rapid progression of the plant-growing season led to greater trophic mismatch between caribou calving and plant phenology (r=−0.77, p=0.07): the per cent of forage species emergent at the date of 50% births was nearly twice as great in the earliest and most rapid spring than in the latest and most gradual spring (figure 3a).

Early caribou calf mortality was closely related to the degree of trophic mismatch around the time of calving (r=0.70, p=0.12). Calf mortality varied sevenfold between the lowest and highest degrees of trophic mismatch observed (figure 3b). Accordingly, calf production declined with increasing trophic mismatch (r=−0.89, p<0.02), varying fourfold between the lowest and highest levels of trophic mismatch observed (figure 3c).

For animals inhabiting seasonal environments, successful reproduction depends on synchronizing offspring production with the time of year when resources are most abundant or of highest quality. In the far north, nutritional content and digestibility of plants reach a peak soon after emergence and decline rapidly thereafter (Klein 1990; Albon & Langvatn 1992). Hence, timing of parturition by caribou and wild reindeer (also R. tarandus) is closely linked to the start of the plant-growing season (Post & Klein 1999; Post et al. 2003). The extent to which onset of parturition in caribou—or in any northern herbivore—can track shifts in plant phenology induced by climatic warming is therefore a key question. While gestation length is fixed at approximately 240 days for this species (Leader-Williams 1988) and the annual reproductive cycle is entrained by seasonal changes in day length (Lincoln & Short 1980), there is some indication that caribou might be able to adjust the timing of their annual reproductive cycle to match, to some extent, changes in plant phenology. For instance, geographical variation in onset and peak of calving among populations of caribou and wild reindeer correlates closely with geographical variation in the timing of the plant-growing season among the areas inhabited by those populations (Skogland 1989). As well, Norwegian reindeer introduced to the sub-Antarctic island of South Georgia completely reversed their annual reproductive cycle by six months within 2 years of introduction, although it would seem this reversal was ultimately driven by the seasonal reversal of day length variation from the Northern to Southern Hemisphere (Leader-Williams 1988).

Of key importance to caribou in this population, however, is the rate at which plant phenology will advance with further changes in spring temperature. Our results indicate that, whereas onset of plant growth is highly variable among years, onset of parturition by caribou is not (figures ​(figures11 and ​and2).2). This would suggest a ‘bet-hedging’ strategy in caribou of timing parturition to coincide with a long-term average onset of favourable conditions. Over the course of our study, an advance in the onset and progression of the plant-growing season by approximately two weeks precipitated an increase in calf mortality and fourfold decline in calf production (figure 3). This two-week advance in plant phenology corresponded to an increase in average spring (March–May) temperature of 4.63°C in our study site over the same period (figure 2). With a further 3–5°C increase in warming expected throughout the Arctic (Maxwell 1997), the extent to which plant phenology will further advance is critically important to the future reproductive success of caribou in this population. The results of a warming experiment we conducted at the same study site indicated that an increase of 4°C advanced phenology of key species, used by caribou at the time of calving, by up to 10 days (Post et al. in press, submitted).

To our knowledge, our results are the first such documentation of a developing trophic mismatch in an Arctic mammal and its consequences for offspring production. While the patterns are clear, our analyses are, in some cases, hampered by low sample sizes. Therefore, our results cannot be considered conclusive. Nonetheless, they corroborate results from better-studied systems with longer-term data documenting the implications of climate change for trophic mismatch in aquatic and marine systems (Edwards & Richardson 2004; Winder & Schindler 2004), and of consequences of trophic mismatch for reproductive success and population dynamics in migratory birds. By far, the best studied of such systems is that of insectivorous birds including great tits (Parus major) and pied flycatchers (F. hypoleuca) in The Netherlands. Insectivorous birds should be especially susceptible to trophic mismatch due to climate change because emergence of their forage species in spring habitats is cued by local temperatures, whereas spring migration by passerines is cued by changes in day length. Great tits, for example, have been shown to suffer mistimed reproduction as climatic warming has advanced the appearance of invertebrate prey but not the timing of their own offspring production (Visser et al. 1998). In pied flycatchers nesting in The Netherlands, the timing of spring arrival on nesting grounds has not advanced in association with warming over the past two decades, whereas timing of egg laying has advanced due to selection pressure on offspring provisioning (Both & Visser 2001). Nonetheless, the advance in laying date has not kept pace with the advance of emergence of key forage species of invertebrates, and the magnitude of decline in several Dutch populations matches the extent of the temporal mismatch between caterpillar emergence and nestling production (Both et al. 2006).