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Mast seeding is defined as the synchronous and highly variable production of seed crops by a population of plants from year to year (Kelly 1994). The critical components of mast seeding are thus both high variability in seed production and high synchrony among individuals. Mast seeding is well documented in a number of plant species, with synchrony detected in seed production between populations over large geographical areas (2500 km for Pinus spp.; Koenig & Knops 1998a). Several hypotheses have been proposed to explain synchronous seeding by individuals within populations, with seed predator satiation and increased pollination efficiency having the most support (reviewed in Kelly 1994; Kelly & Sork 2002). Mast seeding may satiate seed predators such that individual plants experience higher reproductive success (Janzen 1971; Silvertown 1980; Kelly 1994), or increased individual pollination success (reviewed in Kelly & Sork 2002). As individuals become synchronized, selection should act against asynchronized individuals, thereby enhancing selection for high degrees of synchrony (Janzen 1971).
Temporal and spatial patterns of variability and synchrony are also relevant to ecosystems because seed-predator population dynamics, and even community-level dynamics, may be affected by seed crop availability (Ostfeld & Keesing 2000; Koenig & Knops 2001). Spatial variation in synchrony of seed production by individual trees over relatively small scales (< 10 km) has been studied in Quercus spp. (Koenig et al. 1999; Liebhold et al. 2004). Synchrony in acorn production between individuals declined with distance for some species and regions, but not others, and the extent of spatial synchrony was correlated with environmental factors influencing acorn production (Koenig et al. 1999). Here, we examine the variability and synchrony of seed production by 356 individual Picea glauca (Moench) Voss (white spruce) trees separated by distances of 30 m to over 5 km, measured over 16 years. Picea glauca is a wind-pollinated and wind-dispersed mast seeding conifer species whose seeds are a food source for many small mammals and birds (Dale et al. 2001). We address two questions: (i) How variable is seed production between and within years? (ii) How synchronized are patterns of seed production between individual trees? We determine if synchrony between individuals varied with distance between individuals and/or whether or not a mast crop was produced. We show considerable variability in the synchrony of cone production patterns of individual trees, and the tendency for synchrony to decline with increased distance between trees. We explore sources of variability that could affect synchrony among individuals, including variation in the occurrence of mast-years at the plot-scale within which individuals are nested, synchrony in the production of large and small cone crops by individuals within years, and endogenous cycles of individual cone production.
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Overall, individual trees were moderately synchronous in their pattern of cone production, with a mean correlation of 0.52, but this varied with distance between trees. This correlation value is in keeping with ‘moderate synchrony’ used previously to describe mean Spearman and Pearson correlations of 0.53 (Buonaccorsi et al. 2001; Koenig et al. 2003, respectively). Individuals were highly synchronous at the most local spatial scale, and they showed low synchrony at distances over 3000 m. Some of this variation was due to differences detected at the plot-scale, specifically with respect to the occurrence of mast years. Our results suggest that regional mast years can vary in intensity locally, and can affect synchrony of individuals. In 1998 ‘masting’ occurred over all study plots. In 1993, all but one of the plots masted, while in 2005 only half of the plots had a mast cone crop.
Variability among individuals was also detected in the level of synchrony in the production of large cone crops by trees, and in different lags of cone production. The degree of synchrony within a year at the plot level appeared to vary with the magnitude of cone production. Many trees produced large cone crops during mast events. During the 1998 mast, synchrony in the production of large cone crops by individuals was especially high; only 10% of all trees sampled did not produce one of their large cone crops. In the other mast years (1993, 2005) the extent of masting was not as strong, with the percentage of trees within a masting plot that produced large cone crops varying from 36 to 75%. In low cone years, some individuals produced large cone crops that would contribute to the moderate level of overall synchrony. Variability in the number of cones produced among individuals within a year tended to be inversely related to mean cone abundance within the year.
Variation in synchrony among individuals could also be influenced by persistent individual differences in temporal cone production patterns. We detected three dominant patterns of cone production by trees. Some individuals showed no lag in cone production over the years (i.e. each year was independent of those preceding it). Other individuals showed a significant negative effect of cone production in one year on the cones produced the next year; third, those trees producing more mean cones over the study than those in the other groups tended to have a positive autocorrelation at 3-year intervals. P. glauca cones develop over 2 years, with bud differentiation occurring in summer of one year and the cones produced the next year (Nienstaedt & Zasada 1990). Greene & Johnson (2004), in a study of North American tree species, reported 31% of the data sets in their study had significant lag 1 autocorrelations, suggesting it was related to resource depletion, but provided no explanation for variation among trees. Local habitat quality (e.g. basal light availability) influences cone production (Greene et al. 2002), and energy reserve dynamics of individuals could affect their seed production patterns (Satake & Iwasa 2000). In high quality areas trees may have more resources, resulting in both high cone production within a year and allowing trees to produce cones over successive years (Nienstaedt & Teich 1972) and in a multiyear lag in cone production. Habitat variability within sites could be a factor in the variation in synchrony in Quercus spp. mentioned previously (Liebhold et al. 2004). A tendency for a small proportion of trees to produce a large proportion of seed in a population has been shown in Quercus spp. (Healy et al. 1999). Here, the dominant 3-year lag for the high mean cone producing trees coincided with the significant plot-level lag in cone production (for plots A and B; analysis not shown).
While we reported correlation coefficients statistically greater than zero at all distance classes, we focused more on the patterns and relative amounts of synchrony among individuals rather than simply the statistical detection of synchrony. Previous studies have inferred synchrony from a statistically significant positive correlation among individuals (i.e. significantly > 0), regardless of how small and close to zero (Koenig & Knops 1998b, e.g. a correlation of 0.12 ± 0.03 (95% CI); Crone & Lesica 2004). Further information on the amount of variability explained could be attained by squaring the correlation coefficients, while preserving the sign of the Spearman correlation, to generate ‘correlation index’ (r2) values, representing the proportion of variability in the cone production pattern of a tree explained by correlating it with another tree (Zar 1999). The correlation index may be useful for quantifying and interpreting the relative importance of correlations of different magnitudes compared with the correlation coefficient (rs), especially when correlations are not very strong (not close to 1 or –1), nor very weak (not close to 0) (Sokal & Rohlf 1995).
With the correlation index approach, the mean proportion of variation explained for the 356 trees was 0.35 ± 0.12. The spatial pattern of the proportion of variability explained in cone production patterns between pairs of individuals had the same trend as the Spearman correlation (i.e. a decline with distance). The mean proportion of the variation explained ranged from a high of 0.47 ± 0.18 to a low of 0.21 ± 0.06 (see Figure S1 in Supplementary Material). Similar to the Spearman correlation for measuring synchrony, there was no significant reduction in the mean correlation index between pairs of trees in the closest and furthest distance classes (one sided t-test, t623 = 0.981, P = 0.164). The variability in cone production patterns explained by pairs of trees over all distance classes was statistically greater than 0, and there was considerable variation in the cone production patterns of individual trees.
Analyses of 43 Quercus spp. acorn production data sets using mean Pearson correlation coefficients among individuals as measures of synchrony, ranged widely from 0.18 to 0.82 (Koenig et al. 2003). Our mean Spearman correlation was in the middle of this range at 0.52. Spatial synchrony in acorn production between individuals of three Quercus spp. based on Pearson correlations were in the range of 0.60 to 0.35 over distances up to 5 km (Koenig et al. 1999). Although we found no statistical difference in the synchrony of P. glauca trees at 75 m compared with 4 km apart, synchrony did decline with distance to a low of 0.33. Whether synchrony in cone production by P. glauca individuals over larger distances declines further is unknown. Using population means, Koenig & Knops (1998a) found detectable levels of synchrony for Picea spp. populations up to 2500 km apart. Because we focused on the synchrony between individual plants, and not population means, the overall mean correlation based on individuals (0.52) was lower than that based on P. glauca means for populations less than 10 km apart (0.73 here, based on plot means; c. 0.70 from Koenig & Knops 1998a). This occurs at least in part because taking the mean ignores the individual variation by combining individuals in an area into a single value, and suggests that considerable variation may remain undetected when population means, not individual values, are used in the analysis of synchrony.
weather as a cue for synchrony
Broad-scale weather has been suggested as a cue ensuring the majority of trees are synchronous seed producers (Norton & Kelly 1988). Koenig et al. (1999) proposed that the synchronizing effect of weather over large areas, known as the Moran effect (Moran 1953), could be responsible for synchrony in acorn production by Quercus spp. over hundreds of kilometres. Also, abnormally high temperatures in the summer before seedfall, consistent with the La Niña phase of the El Niño Southern Oscillation, has been associated with synchronous fruiting in multiple species across New Zealand (Schauber et al. 2002). Broad weather patterns may also play a role in the detectable levels of synchrony in Picea spp. seeding occurring over large spatial scales (Koenig & Knops 1998a). Bud development in many conifer species occurs a year prior to cone formation, triggered by hot dry conditions during the period of differentiation into vegetative or sexual buds (Owens & Molder 1977; Nienstaedt & Zasada 1990), with a high correlation to the number of pollen cones and seed cones on individual trees (Caron 1995).
Janzen (1971) postulated that for weather to be a synchronizing factor over a large area it must be of a sufficient intensity to override differences due to local conditions. Over the relatively small spatial extent of the current study area we expected that the general climatic conditions favouring the formation of reproductive buds would not differ. However, tree growth and seed output are also affected by soil moisture and competition for resources (Greene et al. 2002), and these are likely to be correlated for individuals close together, leading to patterns of local high synchrony. Perhaps local microsite conditions were such that, if the synchronizing effect of weather must achieve some threshold to override local microsite variation (as per Janzen 1971), the conditions leading up to the 1998 mast were well above the threshold (so all areas had a cone mast), whereas weather conditions in 1993 and 2005 were nearer the threshold, such that the occurrence of cone masting was more variable between plots. Accordingly, no mast years occurred in other years perhaps because the large-scale cue was not present. The spatial variation in mast years among plots, and variability in individual synchrony, could reflect the variation in habitat conditions (Liebhold et al. 2004) when these conditions are not overridden by weather for mast seeding. We do not know the cause of the variation in mast occurrence among plots. Local moisture or frost conditions during the very short time of pollen shedding (3–5 days; Nienstaedt & Zasada 1990) could negatively affect synchronization of masting. We did not have climatological data to pursue this further. The broad scale patterns showing some detectable level of synchrony in population means observed over very large distances (e.g. Koenig & Knops 1998a) could result from large-scale climatic conditions that trigger a mast year across sites over large distances, with considerable variation in the other years.
pollination efficiency and predator satiation
It was not our goal to differentiate between evolutionary hypotheses for mast seeding, so we only briefly comment on pollination efficiency and predator satiation in light of our results on variability and synchrony. The high CVp and mean CVi, along with high local mean rs, could be the response to selection due to local pollination efficiency and localized seed predators (Koenig et al. 2003). Picea glauca pollen is wind dispersed; most pollen from wind-dispersed conifers has been shown to fall closer to the source tree (Robledo-Arnuncio & Gil 2005), and could result in individuals closer together being more synchronous. This could reinforce via heritability the different patterns of lags observed in cone production, perhaps reflecting different seed production strategies or abilities. Genetics may also play a role in the mast seeding behaviour of P. glauca individuals (Nienstaedt & Zasada 1990), but we do not have the data to test this idea further. As the only conifer in our study area, P. glauca should experience strong selection to be synchronous due to predation pressure. However, this selection is likely to be influenced by the attributes of predator species. If the dominant seed predator was highly mobile, then very high synchrony in seed production may occur over the range of the seed predator. Red squirrels are territorial and thus do not roam in search of food, unlike birds such as crossbills (Holimon et al. 1998). Red squirrels feed primarily on P. glauca seed (Smith 1968) and individuals cache upwards of 12 000 cones prior to seedfall (Hurly & Lourie 1997), preferentially selecting cones from trees with larger cone crops (Peters et al. 2003). Seeds lose their viability after 1–2 years in a red squirrel cache (Nienstaedt & Zasada 1990). Therefore, while selection should act against individual trees producing large cone crops asynchronously, this may only be important in a local area, for example within a red squirrel territory (0.25 ha, or a diameter of about 60 m; J. M. LaMontagne & S. Boutin, unpublished data). This may contribute to the high level of synchrony among individuals in the closest proximity (< 75 m). Increased asynchrony with distance, resulting in areas where trees produce many cones when other trees produce small cone crops, may promote seed predator persistence, especially in low seed years. However, mobile generalist seed predators may show the opposite of predator satiation (i.e. higher proportion of the seed crop consumed in high seed years or for high-seed trees), as shown for Betula allegheniensis (Kelly et al. 2001). Under the latter conditions it might be more favourable for individual plants to be highly variable (high mean CVi) with lower spatial synchrony to tailor the amount of variation and its spatial scale to the characteristics of its seed predator(s), as outlined by Koenig et al. (2003).
Although statistically detectable synchrony in seed production by plant populations may extend over very large spatial extents, individual variation in cone production patterns may be considerable. Different species and even different populations of a common species will experience different local environmental conditions and selection pressures via the characteristics of seed predator populations and developmental times (e.g. promoting asynchrony between different species of Quercus spp. in a common area; Liebhold et al. 2004). Based on high local synchrony, high synchrony within a mast year, and multiple lags in cone production by individuals, both available resources and strong weather cues appear to play roles in the observed patterns. Spatial variation in the occurrence of mast years can have an affect on the population dynamics of seed predators and local community dynamics (Ostfeld & Keesing 2000). There is much opportunity to investigate further the causes and consequences of individual variation in synchrony, and individual lags in seed production, with a view to increasing our understanding of seeding patterns within plant populations.