- Top of page
- Materials and Methods
- Supporting Information
A fundamental tenet in life history theory is that tradeoffs among vital rates in organisms arise because resources are finite and preferential allocation to a given function reduces resources available for other competing functions (Williams, 1966; Roff, 1992). In plants, for instance, costs of reproduction are very common (Obeso, 2002). Although limiting resources are the physiological basis of life history trade-offs, emphasis in the literature for wild plants has been on either documenting the demographic costs or quantifying several interrelated measures of proportional resource allocation to reproduction and subsequent effects on vegetative growth (see Obeso, 2002 for a review). By contrast, few studies have directly measured the degree to which reproduction depletes stored resources (i.e. measurements of storage) in wild plants (Cipollini & Stiles, 1991; Newell, 1991). Such data are especially relevant for long-lived, large plants that can store a significant amount of resources and retrieve them during times of demand (Chapin et al., 1990). If storage pools are large enough to meet competing demands, the short-term costs of reproduction on growth may not be detected, although depletion of stored resources may lead to longer term costs. In this case, a more meaningful measure of the direct costs of reproduction is the degree of stored resource depletion (Reznick, 1985; Ehrlen & Van Groenendael, 2001).
Resource depletion is expected to be particularly high in masting species, which are characterized by the synchronous and intermittent production of large seed or fruit crops (Herrera et al., 1998; Kelly & Sork, 2002; Crone et al., 2011). Indeed, preferential resource allocation to reproduction during mast events has long been thought to deplete storage pools and to require a replenishment period with low reproductive output before the next mast event (Janzen, 1974; Harper, 1977; Rathcke & Lacey, 1985; Kelly, 1994; Newbery et al., 2006). Consistently, resource depletion is a key assumption of theoretical models to explain masting patterns (Yamauchi, 1996; Satake & Iwasa, 2000; Masaka & Maguchi, 2001; Rees et al., 2002; Satake & Bjørnstad, 2008). While depletion of stored resources has been shown in orchard species that are bred for increased fruit yield (Goldschmidt & Golomb, 1982; Brown et al., 1995; Rosecrance et al., 1998), empirical direct data for wild plants (Crone et al., 2009) are very rare. Direct data on resource depletion in wild masting trees exists only for carbohydrates, and the evidence is mixed and species-specific, with no effects in some species (Hoch et al., 2003) and tissue-specific depletion in other species (Miyazaki et al., 2002; Ichie et al., 2005). These mixed results likely reflect the fact that carbon is not necessarily the best currency to measure costs of reproduction (Ashman, 1994; Hemborg & Karlsson, 1998), particularly if plants compensate for carbon demands during reproduction (Reekie & Bazzaz, 1987a), or if carbon does not necessarily limit growth in the short term (Körner, 2003; Sala & Hoch, 2009).
Compared to carbohydrates, mineral nutrients, particularly nitrogen (N) and phosphorus (P), may be a more appropriate currency because they are usually limiting in the environment and because reproductive structures (particularly seeds and fruits) are generally nutrient enriched relative to vegetative biomass (Reekie & Bazzaz, 1987b). Convincing evidence for depletion of stored nutrients after mast events exists only for orchard trees (Goldschmidt & Golomb, 1982; Brown et al., 1995; Rosecrance et al., 1998). In wild trees, by contrast, such evidence is rare and more indirect. For instance, nutrient allocation to reproductive structures during mast events has been related to strongly phosphorus-depleted litter in some species (Newbery et al., 1997), and to nutrient-limited flower primordia development in others (Han et al., 2008). In both cases, reproduction is hypothesized to deplete within-tree nutrient reserves, but direct measurements were not available. By contrast, Yasumura et al. (2006) reported no nutrient-depleted litter after a mast event, although their results are equivocal due to limitations of the study design.
The assessment of costs of reproduction in trees is further complicated by the fact that trees are modular organisms where branches operate as semiautonomous units (Watson & Casper, 1984; Lovett-Doust & Lovett-Doust, 1988; Sprugel et al., 1991) and costs of reproduction may vary depending on the modular level examined (Obeso, 1997). With respect to carbohydrate demands, branch autonomy has been shown to be species-specific, with some species showing complete autonomy (Hoch, 2005) and others relying to a variable degree on carbohydrate import from other parts of the tree (Obeso, 1998; Miyazaki et al., 2002). However, branches cannot be indefinitely autonomous with respect to mineral nutrients. Depending on the overall nutrient demand for reproduction, nutrients may be drawn from branches bearing reproductive structures only (local depletion) or from other equivalent branches regardless of reproductive status (nonlocal depletion). Whether resource depletion is local vs nonlocal is likely to influence temporal patterns of reproduction. Under local resource depletion sexually mature branches that did not reproduce in a given year may have enough resources to reproduce the subsequent year. Therefore, individuals may be able to reproduce to some degree every year leading to lower inter-annual variation of reproductive output. By contrast, if reproduction in a given year causes all branches to become resource-depleted regardless of their reproductive status (nonlocal resource depletion), then we expect strong decreases of reproductive output after years with high seed set, which is the typical pattern in masting species. In spite of the fundamental, and often invoked, role of stored nutrients in wild masting trees, there are few convincing data on nutrient depletion in standing biomass during and after masting events, as well as on the degree to which costs of reproduction are local vs nonlocal.
Here, we document reproductive output and stored resource dynamics in Pinus albicaulis (whitebark pine), a high elevation masting pine. Specifically, we examine the timing (during and after a masting event) and magnitude (local vs nonlocal) of resource depletion. From the onset of an unusually heavy mast event in 2005, we compared seasonal changes in leaf and branch sapwood N and P concentrations and leaf photosynthetic rates in cone-bearing branches, branches not bearing cones, and branches where we removed cones. To test the timing and magnitude (local vs nonlocal) of resource depletion we compared nutrient concentrations in cone branches and branches that had never had cones. We also examined the consequences of masting for short-term growth by measuring new shoot growth during the mast event and tree ring growth from 1995 to 2010. Specifically, we addressed the following two main questions: does cone maturation deplete nutrients in reproductive branches (local-level depletion)? and, to what extent is nutrient depletion during and after the mast event local vs nonlocal (at the branch- vs the individual-level)? We also explored whether masting was associated with a short-term growth decline. Because whitebark pine produces very large, nutritious seeds (Lanner & Gilbert, 1994), we hypothesized that years of high reproductive output would incur significant nutrient costs with negative physiological consequences. We also hypothesized that if resource switching between reproduction and storage influences future reproduction, then nonlocal resource depletion should occur at some point after the mast event.
- Top of page
- Materials and Methods
- Supporting Information
Although mast events have long been thought to cause a depletion of storage resource pools in plants (see the Introduction section), direct empirical data for wild trees is lacking (for nutrients) or inconclusive (for nonstructural carbohydrates). For whitebark pine, we show that a heavy mast event depleted stored nutrients. Initially (during the mast year), nutrients were depleted locally (in reproductive branches only), but by the subsequent year nutrient depletion was also observed at the individual level (in all terminal branches, regardless of their reproductive status). Our results provide direct evidence of a decline of stored nutrients after a mast event in a wild tree. This is consistent with data from orchard alternate-bearing trees (Goldschmidt & Golomb, 1982; Brown et al., 1995; Rosecrance et al., 1998), and suggests that nutrient depletion is not unique to species specifically bred for high crop yield. Results are also consistent with nitrogen-limited flower bud development after mast events (Han et al., 2008) and with indirect evidence based on nutrient-depleted litter (Newbery et al., 1997). Together, these results support the argument that mast events in wild trees impose a replenishment period before a subsequent mast event.
Nutrient depletion was based on concentrations, rather than total resource pools. Therefore, declines in concentration could, in principle, reflect dilution due to an increase of biomass. However, in our system, this is highly unlikely and probably unrealistic. Based on biomass allocation equations (Callaway et al., 2000), the annual biomass increment of a 38-cm DBH whitebark pine tree (the average diameter of our sampled trees) is 1.4% of the total standing biomass. In the present study, decreases in nutrient concentrations ranged from 13% to 72% (Table 2), depending on the nutrient and tissue fraction, which is at least one order of magnitude greater than the average annual biomass increment.
In whitebark pine, cone production in 2005 was unusually high. Similar cone crops in the region were recorded only once in the past 15–20 yr (Crone et al., 2011; Interagency Grizzly Bear Study Team, unpublished). At our site, cone scar analysis also indicated that cone crops in the past 10 yr were low (Crone et al., 2011). Accordingly, the CVp of seed mass and seed number based on only 5 yr (1.85 and 1.56, respectively) are at the very high end of the CVp range reported for other pines (maximum 1.8; Herrera et al., 1998). Given the high cone crop in 2005 and the large and nutritious seeds of whitebark pine (Fig. 3; Lanner & Gilbert, 1994), the substantial nutrient depletion (between 14% and 72%, depending on the nutrient and tissue fraction; Table 2) is not surprising. Interestingly, depletion occurred incrementally over time: by the end of the masting season resource depletion was local (reproductive branches), but by the end of the next season nutrient depletion was at the individual level (in all terminal branches, regardless of their reproductive status during the mast event). This switch from local to nonlocal nutrient depletion suggests complex resource dynamics after masting in trees and highlights the importance of evaluating reproductive costs over time and at the individual level.
Depletion in cone-bearing branches during the 2005 mast season occurred only in tissues where nutrient concentrations before cone maturation were significantly higher than that in nonreproducing branches (young needles became N depleted and branch sapwood became N and P depleted). Cipollini & Stiles (1991) and Karlsson (1994) also reported higher resource concentrations in reproductive branches before fruit maturation. Because we did not sample before the mast event we cannot tell whether higher nutrients in reproductive branches contributed to cone initiation or the reverse. In any case, nutrient storage in cone-bearing branches was not sufficient to meet reproductive demands and by the subsequent season nutrients were depleted in all branches. A possibility is that the depletion in 2006 was caused by factors other than the mast event. However, this seems unlikely. First, 2006 was a year of near average annual precipitation (572 mm) but above average temperatures (2.8°C). This suggests that nutrient availability in 2006 was not limited by low water or cold temperatures. Second, radial growth data does not suggest any unusual growth pattern in 2006 that could have altered nutrient dynamics. On the contrary, in subalpine pines, tree ring growth is generally stimulated by warmer temperatures (Salzer et al., 2009) as it appeared to be the case in 2003. Thus, it could be that the lack of growth stimulation in 2006 reflects nutrient limitations induced by masting in 2005. Our results are consistent with those of Han et al. (2008) suggesting that nutrient limitation impeded flower bud primordial development after a mast event. Newbery et al. (1997) also documented P-depleted litter after a mast event and hypothesized that reproduction depleted within-tree P reserves. However, direct evidence of nutrient depletion (in standing biomass) was not available in either case and alternative explanations are possible. For instance, litter-based inferences may be limited by the degree to which nutrient resorption offsets nutrient demands for reproduction and buffers changes in storage. Unless critical resource thresholds for reproduction are very low, the nutrient depletion we document suggests that a period of nutrient replenishment followed by appropriate climate cues is required before a subsequent mast event (Smaill et al., 2011).
Most of the few studies on resource costs of mast-seeding in trees have focused on nonstructural carbohydrates and results have been mixed (Miyazaki et al., 2002; Hoch et al., 2003; Ichie et al., 2005). This may reflect in part the degree to which current photosynthate production by foliage (and sometimes by reproductive structures) compensates for carbon demands by reproduction (McDowell et al., 2000; Obeso, 2002; Ichie et al., 2005). In contrast to nonstructural carbohydrates, nutrients are often considered a better currency to measure costs of reproduction in plants (Ashman, 1994; Hemborg & Karlsson, 1998). In trees, this is particularly true because carbon is often not limiting growth in the short term (Körner, 2003; Millard et al., 2007; Sala & Hoch, 2009), as is the case for whitebark pine (Sala et al., 2011). In addition, individual branches cannot be indefinitely autonomous with respect to nutrients (Sprugel et al., 1991). Further, whitebark pine occurs in subalpine habitats (Tomback et al., 2001) where short-term growth and reproduction are often nutrient- (Bowman et al., 1993; Karlsson, 1994) but not carbon-limited (Hoch et al., 2003; Hoch, 2005). The investment of leaf N to reproduction in cone-bearing branches at the cost of C assimilation via photosynthesis is consistent with nutrient- but not C-limited reproduction. In contrast to other results (Wheelwright & Logan, 2004), this apparent C cost did not affect new shoot or radial growth also suggesting that C does not limit growth in the short term. Current resource dynamics models to explain masting patterns are based on stored photoassimilates (Isagi et al., 1997; Satake & Iwasa, 2000). Our results for whitebark pine indicate that these models should be interpreted more generally as dynamics of stored resources (carbohydrates and/or nutrients), depending on what resources limit reproduction in different species. For example, depletion of carbohydrates, but not nutrients, followed mast years in a mast-seeding perennial wildflower (Crone et al., 2009) suggesting that carbon may be more limiting in herbaceous than in woody plants.
Relative N depletion was roughly similar in needles and branch sapwood while relative P depletion was greater in branch sapwood than in needles. However, much lower nutrient concentrations in branch sapwood translated to higher absolute N extraction from foliage relative to sapwood and roughly similar P extraction from both fractions (Table 2). Therefore, foliage contributed proportionally more N, but not P, to reproduction than branch sapwood, which may reflect a greater surplus of N relative to P. This is consistent with the proposed N storage function of the carboxylating enzyme rubisco in leaves of trees (Millard et al., 2007), with P-limited growth in whitebark pine (Perkins, 2004), and with the importance of P acquisition for reproduction in other masting trees (Newbery et al., 2006). Interestingly, a major peak of P allocation to seeds (but not N) was observed later in the season, which coincided with a slight decrease of P concentration in older needles from late August to late September. It may be that such ‘last minute’ allocation of P to seeds is a strategy to maximize P use or to prevent premature P loss to seed predators such as red squirrels (Tomback et al., 2001). The role of foliage as a nutrient source for reproduction is consistent with the hypothesis that the unusual proportional increase of leaf biomass with tree size in whitebark pine is a strategy for nutrient storage for reproduction at the cost of water loss and carbon assimilation (Sala, 2006). The storage role of foliage is also consistent with increases in litter fall after mast seeding in Himalayan oaks (Singh et al., 1990) and in Nothofagus species (Alley et al., 1998). This is because nutrient re-allocation from foliage to reproduction could trigger leaf senescence if nutrient levels fall below critical thresholds to sustain a positive leaf carbon balance (Reich et al., 2009).
Although nutrient costs of reproduction decreased photosynthetic rates in reproductive branches in 2005, short-term growth at the branch or the tree level was not affected. Rather, nutrient depletion was followed by reduced future reproduction. This pattern in whitebark pine is consistent with that in other species where resource switching during reproductive events occurs between storage and reproduction rather than between growth and reproduction (Stearns, 1989; Ehrlen & Van Groenendael, 2001). Apparently, at our site, factors other than reproduction influenced radial growth because no heavy mast event occurred since at least 1995 (Crone et al., 2011), but tree ring growth decreased from a high peak in 2003, a year with higher (11.2°C) than average (9.5°C) June and July temperatures (but near average precipitation), to 2004, a year whose June and July temperature (9.47°C) and precipitation (30 mm) were near average (34 mm). These fluctuations probably reflect the combined effect of climatic and internal factors, although our short tree ring growth series did not reveal significant relationships between tree ring growth and climatic variables. Interestingly, mature cones in 2005 (mast year) were initiated following a warm year in 2003, which is consistent with previous findings that relatively high temperatures cue mast seeding in tree species (Selas et al., 2002). Resource switching between storage and reproduction during reproductive events may operate in other mast-seeding tree species for which tradeoffs between growth and reproduction have not been detected (Despland & Houle, 1997; Yasumura et al., 2006; Knops et al., 2007).
True masting (Kelly, 1994), a distinct bimodal pattern of reproductive output with years of very high seed production interspaced between years of no or minimal reproduction, is rare in plants, and most species fall somewhere along a continuum from true masting to random variation in reproduction through time (Herrera et al., 1998). In our study region, whitebark pines span a broad range of variability along this continuum (Crone et al., 2011). Past studies (see review by Kelly & Sork, 2002) have tended to explain variability in masting in terms of variation in the costs of reproduction and the presence of external synchronizing factors such as pollen availability, drought and temperature. Recent work also indicates that the effect of some synchronizing climatic cues may be mediated via changes in nutrient availability (Smaill et al., 2011). Our results further suggest that differences in mast-seeding could also be caused by the extent to which nutrient depletion is synchronized within individuals. For example, if costs of reproduction are moderate (e.g. where or when nutrient availability and resource storage is high) resource depletion may tend to be more localized (and therefore less synchronized within a tree) in which case subsequent reproduction may occur in branches that did not reproduce the year before, thus reducing annual variation in reproductive output. This is consistent with the prediction by Kelly & Sork (2002) that the coefficient of variation of seed fall should be lower in more productive habitats.