Over the course of the study, the mean (±1 s.d.) date of onset of the plant-growing season (the date of emergence of 5% of species) was 22 May (Julian day 142; ±8.9 days), whereas the mean date of onset of the caribou calving season (the date of 5% births) was 3 June (Julian day 154; ±3.6 days; ). Between 1993 and 2006, the timing of onset of the plant-growing season (estimated as the date of emergence of 5% of plant species) advanced by 4.59 days; for the subset of those years for which data are continuous (2002–2006), onset of the plant-growing season advanced by 14.8 days (: open circles). By contrast, between 1993 and 2006, timing of onset of calving (date of 5% births) advanced by 3.82 days; whereas from 2002 to 2006, when advancement of the plant-growing season was most pronounced, onset of calving advanced by only 1.28 days (: solid circles). Moreover, interannual variability in onset of plant growth (CV=6.28) was approximately twice as great as that of caribou calving (CV=2.34), though this difference was not significant (F5,5=2.69, p>0.50). Taken together, these results suggest that caribou display less interannual variability in the timing of their reproductive cycle than do the forage plants upon which they depend for offspring provisioning at the period of peak resource demand. They furthermore indicate a rapidly developing mismatch between caribou reproduction and the timing of availability of their forage ().
Figure 2 Dates (in day of year) of emergence of 5% of forage species (open circles, dashed line) and of 5% of caribou births (filled circles, solid line) at the study site in Kangerlussuaq, West Greenland, during the period of continuous annual data collection (more ...)
Among years, the timing of onset of the plant-growing season was most closely related to mean April temperature (r
=0.20). Timing of onset of caribou calving displayed its strongest correlation to mean spring (March–May) temperature (r
=0.12). Onset of calving was not, however, closely correlated with that of the plant-growing season (r
>0.50), presumably because, as noted above, the onset of plant growth was considerably more variable among years than was the onset of calving (). Mean spring temperature, over the course of the study, increased by 4.63°C, though the correlation with ‘year’ is only marginally significant (r
=0.058). 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 (a
), our nonlinear regression estimates of the beginning of the growing season each year are less precise than those of the onset of calving (b
). 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 (a).
Figure 3 (a) Relation between the midpoint of the plant-growing season and the index of trophic mismatch between caribou calving and plant phenology each year; an earlier occurrence of the midpoint of the plant-growing season leads to greater trophic mismatch. (more ...)
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 (b). 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 (c).
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 and ). 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 (). 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 (). 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
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
The example of population declines in pied flycatchers illustrates the consequences of mistimed reproduction in migratory species that are unable to fully compensate through adjustments in their reproductive phenology for climate-driven changes in the timing of availability of resources. We might expect intense selection for earlier reproduction in caribou and other Arctic herbivores if further climatic warming and greater trophic mismatch reduce reproductive success. Some of the female reindeer introduced to the island of South Georgia, for instance, were pregnant and produced offspring in their first May on the island; their calves, however, died because their birth coincided with the onset of winter on the island (Leader-Williams 1988
). Nonetheless, those same females eventually adjusted their reproductive cycles to coincide with the sub-Antarctic seasons, and reindeer persist there today (Leader-Williams 1988
). We suggest, however, that the role of trophic mismatch in reproductive success and population dynamics of this and other Arctic species warrants urgent attention.