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Carnivory is one adaptation to enhance nutrient acquisition, that is utilized by a small set of plant species of infertile habitats (Givnish 1989). The benefits of carnivory (see review by Adamec 1997) include increased growth, higher flowering frequency, seed mass and nutrient concentrations (Aldenius et al. 1983; Karlsson et al. 1991; Thorén & Karlsson 1998) and increased survival (Zamora et al. 1997) in plants that succeed in catching prey. Furthermore, it has been suggested that prey capture may increase soil nutrient uptake in carnivorous plants (Aldenius et al. 1983; Hanslin & Karlsson 1996; Karlsson et al. 1996). In species of the genus Pinguicula, the nitrogen (N) gain through prey capture has been estimated to range between 15% and 40% and between 7% and 26% of the annual N loss of non-reproductive and reproductive plants, respectively (Karlsson et al. 1994), thus reducing the amount of N that has to be taken up from the soil. However, the high variation of seasonal catches among individuals and years (Karlsson et al. 1994) renders carnivory an unreliable source of nutrient income.
On the other hand, carnivory in plants is probably also associated with considerable costs (Benzing 1987), for instance when leaves are used for both carbon assimilation and prey capture. This may, for example, lead to reduced photosynthetic production per unit leaf nitrogen when carnivorous Pinguicula species are compared with non-carnivorous species in similar environments (Méndez & Karlsson 1999). Such costs might be the cause of the relative rarity of carnivory, at only about 0.2% of all vascular plants, i.e. 500–600 species (Givnish 1989). The low competitive ability of the mostly small carnivorous plants further suggests that they should be restricted to habitats where water and light are abundant but nutrient availability is low (Givnish et al. 1984; Karlsson et al. 1991, 1996).
Although aspects of the resource economy of carnivorous plants have been studied (e.g. Karlsson 1988; Thum 1988; Karlsson et al. 1991; Thorén 1998) none, to our knowledge, has directly related their performance (in terms of productivity) to the flux of growth-limiting nutrients (uptake or loss). Applying the concept of nutrient use-efficiency (NUE) (Berendse & Aerts 1987; Garnier & Aronson 1998) to carnivorous perennials could shed further light on the consequences of carnivory and reproduction on plant nutrient dynamics. The separation of NUE into the productivity per unit nutrient (annual nutrient productivity, aNP) and the mean residence time of nutrients (MRT) as defined in the concept of Berendse & Aerts (1987) allows for a functional interpretation of NUE in terms of different nutrient use strategies (Eckstein & Karlsson 1997; Berendse 1998).
The principle of allocation (Willson 1983; Silvertown & Lovett Doust 1993) is based on the assumption that different plant functions compete for a limited resource pool. Reproduction should therefore incur a cost that is expressed as negative consequences either on growth (somatic costs) or future survival and fecundity (reproductive costs, cf. Stearns 1992). In general, empirical studies on costs of reproduction have not found consistent results (e.g. Reekie & Bazzaz 1987; Horvitz & Schemske 1988; Obeso 1993; Syrjänen & Lehtilä 1993). For the genus Pinguicula, however, significant costs of reproduction have been identified in both somatic (Thorén et al. 1996) and demographic terms (Svensson et al. 1993), with survival probabilities significantly reduced in reproductive individuals. In infertile environments a cost of reproduction could be mediated by flower and seed production accelerating nutrient turnover, leading to increased nutrient losses that cannot be replenished by uptake from the soil.
To test for the proposed link between reproduction and nutrient turnover we studied the effect of reproductive status on N use-efficiency (NUE) of three species of Pinguicula–P. alpina L., P. villosa L. and P. vulgaris L. – under field conditions. The reproductive allocation in terms of N, i.e. the proportion of the total N pool allocated to reproductive structures, is on average 0.3, 0.6 and 0.4 for P. alpina, P. villosa and P. vulgaris, respectively (Karlsson 1988; Karlsson et al. 1990; Thorén et al. 1996; Hemborg & Karlsson 1998). Although reproductive plants usually have larger biomass and nutrient pools than vegetative plants during the growing season, they also lose more nutrients through senescing reproductive structures in the autumn (Karlsson 1986, 1988; Thorén et al. 1996). Winterbuds are therefore usually smaller and contain less N after flowering than those of non-reproductive plants. This fact is expressed as a relative somatic cost of reproduction (RSC, Thorén et al. 1996).
The mean residence time of nutrients (MRT) is defined as the ratio between the average nutrient pool and the annual nutrient losses, and nutrient productivity (aNP) is the ratio between annual production and the average nutrient pool (Berendse & Aerts 1987; Aerts 1990; Garnier & Aronson 1998). Since both components of NUE are ratios, it is not obvious how reproduction will affect MRT and aNP but we hypothesize that it may lead to a proportionally larger increase in N losses than in average N pool size. Increased N turnover (lower MRT) in reproductive plants would lead to a higher annual N requirement and thus explain the negative effects of flowering on future fate unless this can be compensated for by soil- or prey-derived nutrients. We test whether N use-efficiency of reproductive plants is indeed lower than in non-reproductive individuals.
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In general MRT and NUE of subarctic Pinguicula is comparable to published data on N retention of non-carnivorous herbs (cf. Eckstein et al. 1999). Thus the carnivorous study species share a similar N use strategy with other herbs and graminoids.
The photosynthetic NUE, i.e. the photosynthetic rate in relation to leaf N content, of the three Pinguicula species (Méndez & Karlsson 1999) shows similar ranking among species as the whole-plant NUE of the present study; P. alpina having c. 55% higher photosynthetic NUE than P. villosa. However, these carnivorous plants showed lower photosynthetic NUE than non-carnivorous species. Photosynthetic NUE is one component of the annual nitrogen productivity (Garnier et al. 1995) and thus part of a wider whole-plant-based NUE approach (Garnier & Aronson 1998).
There is considerable variation in temperature and precipitation between years in the study region (Holmgren & Tjus 1996) that may have an impact on plant growth, nutrient uptake and prey abundance for carnivorous species. Differences in N pool and dry mass productivity among years in the present study are probably related to this climatic variation. Since plant growth in high-latitude ecosystems may be constrained by a number of environmental factors such as N availability, temperature or precipitation (Chapin & Shaver 1985), the relative importance of these may also vary among years (e.g. Weih & Karlsson 1997).
The effect of reproductive status on nutrient turnover
Owing to the loss of seeds, petals and senescent reproductive structures, N losses in reproductive individuals were two to three times higher than losses in non-reproductive plants (Table 1). In contrast, N losses due to leaves and budscales were relatively similar in reproductive and non-reproductive plants. These data confirm that in these plants reproduction considerably influences the N budget of the plant. This is significant especially in nutrient-poor habitats, where lost N can not easily be replenished by uptake from the soil. Can reproductive individuals compensate for this high N investment into reproduction by accumulating a higher average N pool or by resorbing nutrients more efficiently from senescing tissues than non-reproductive plants? In our study the average annual N pool of reproductive plants was smaller than that of non-flowering individuals in all three species (Table 2). Also during the actual growing season there was not a large effect of reproductive status on plant N pool size (Fig. 1). This is in line with the results of earlier studies, where only small differences in the allocation of biomass and N to somatic structures (leaves plus roots) between flowering and non-reproductive individuals of the study species was found (Karlsson 1986, 1988).
Average REFF of the study species of between 40% and 67% (Table 4) matched with values found for a large number of plant species of different life-forms (Aerts 1996). No statistically significant differences in REFF between reproductive and non-reproductive plants were found (Table 3). However, there was a trend towards reproductive individuals resorbing equal or larger amounts of N from senescing leaves than non-reproductive plants (Table 4). Owing to the larger N content in green leaves of reproductive plants, their senescent leaves mostly showed equal or higher N concentrations (RPROF) than those of non-reproductive individuals (Table 4). Resorption from reproductive structures could not be estimated as N loss due to shed seeds could not be separated from possible N resorption from capsule and stalk. However, we may expect that N from reproductive structures would be allocated to developing seeds as these probably represent a strong sink for nutrients.
These observations do not provide any support for a compensation of higher N losses in reproductive plants through an increased N pool size or improved N resorption. This leads in turn to a considerably lower MRT in reproductive individuals as compared with non-reproductive plants (Table 2). In reproductive plants annual N losses were larger than the average N pool size so that each unit of N remained within the plant for less than 1 year (Table 2). It appears that such an impaired nutrient budget may have severe consequences on future survival and growth.
Within reproductive plants of the morphologically similar study species, the ranking in terms of reproductive allocation was consistent with the ranking of species in terms of NUE and its components (Fig. 2). Higher investment into reproduction thus led to both a lower MRT and aNP and resulted in a less efficient N use. Since MRT and aNP decreased with increasing reproductive allocation, there was no trade-off between these two variables among the study species. Our results thus shed some light on earlier empirical data on the effect of reproduction on growth, survival and fecundity. There are significant somatic costs of reproduction (RSC) in P. alpina, P. villosa and P. vulgaris, but these are smaller than the reproductive allocation of the species (RE) (Thorén et al. 1996).
Figure 2. Mean residence time (MRT, upper panel), annual nitrogen productivity (aNP, middle panel) and nitrogen use-efficiency (NUE, lower panel) in relation to reproductive allocation of three species of Pinguicula during 2 years. Open symbols = 1996; filled symbols = 1997; squares = P. alpina; triangles = P. villosa; circles = P. vulgaris.
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The fact that RSC < RE in all species indicates that there should be some sort of compensation mechanism at work (Thorén et al. 1996). N uptake from soil or prey to meet the larger N requirements of reproductive individuals may be facilitated by higher prey trapping success of reproductive plants (vs. non-reproductive) of P. vulgaris (Karlsson et al. 1994). For P. alpina, its perennial root system that allows for rapid growth during the early part of the growing season when nutrients presumably are in good supply may compensate for some of the extra investment into reproduction. Furthermore, reproductive plants of P. alpina showed a higher photosynthetic NUE than non-reproductive individuals (Méndez & Karlsson 1999). However, the presumed compensation is not achieved through a higher N pool or N resorption from senescing leaves in reproductive plants. Hence, evidence for demographic costs of reproduction were found in all three species (Svensson et al. 1993) with survival probability considerably reduced in reproductive individuals.
P. villosa presents some sort of an unsolved paradox. This tiny plant possesses a small annual root system consisting of an average of two unbranched roots of a total length of 20 mm. Still it occurs in the most infertile habitat (on Sphagnum fuscum hummocks) and displays the highest reproductive allocation of the three study species. P. villosa shows the lowest frequency of repeated flowering of the study species and has the shortest population half-life (Svensson et al. 1993). There may be at least two explanations for the apparent paradox. (i) By allocating more resources to reproduction and increasing seed output at the expense of future survival and growth, species may escape these unfavourable conditions and approach a ‘functionally’ monocarpic life-history. (ii) Explanations for the evolution of reproductive allocation can not only be found at the individual or population level. Theoretical models predict that in a metapopulation context with local extinctions an evolutionary stable strategy should favour a high reproductive allocation in unproductive habitats (Ronce & Olivieri 1997).