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Keywords:

  • Curculio elephas;
  • Curculio glandium;
  • Mediterranean oak forests;
  • multi-host–predator system;
  • Quercus humilis;
  • Quercus ilex;
  • seed ecology;
  • seed satiation;
  • species coexistence

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. Pre-dispersal seed predation (PSP) often occurs in multi-host–predator systems (e.g. several plant species exposed to a common array of granivorous insects). However, whether the interaction among seed phenology, seed size and predator size accounts for interspecific differences in PSP remains elusive.

2. We studied PSP in a mixed-oak forest with two oaks (the larger-seeded Quercus humilis and the smaller-seeded Q. ilex), both depredated by two acorn weevils (the smaller Curculio glandium and the larger C. elephas). We intensively monitored acorn production and infestation phenology and we identified the weevil species depredating acorns by means of DNA taxonomy.

3. The minimum acorn size required for infestation was lower for C. glandium than for C. elephas, in accordance with their different body sizes. This resulted in an earlier infestation phenology in C. glandium and the ability of this species to infest both smaller and larger acorns. Above a minimum acorn size threshold, no selection for larger acorns by weevils was observed.

4. Initial acorn crop size was similar in the two oaks. Nonetheless, the earlier acorn phenology and the production of larger acorns in Q. humilis favoured the earlier infestation by C. glandium and the predation by both small and large weevils. Smaller acorns of Q. ilex almost excluded infestation by the larger C. elephas.

5. Although larger acorns of Q. humilis could better survive infestation (preserve the embryo), higher PSP in this species finally resulted in a lower mature acorn crop size than in Q. ilex.

6. Synthesis. In a multi-host–predator system, smaller-seeded species may benefit from a reduced PSP because they exclude larger granivorous insects, but also by means of a ‘free-rider effect’, if larger-seeded heterospecifics earlier reach a critical size to be depredated. These results also highlight the benefits of a small body size in granivorous insects to depredate seeds earlier and to forage on a wider range of seed sizes. Whether the advantage of ‘being small’ in this antagonistic plant–animal interaction is offset by other processes, or whether it results in a pressure towards seed and insect size reduction, deserves further attention.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Pre-dispersal seed predation (PSP) can significantly constrain plant recruitment by reducing the number of viable seeds (Crawley 2000; Siepielski & Benkman 2008). As a result of this remarkable fitness consequence, plants have evolved a wide array of traits to minimize the negative effects of seed predation. These traits have been classified as resistance and tolerance mechanisms (Stowe et al. 2000). Resistance mechanisms preclude seed consumption and include physical barriers and chemical defences (Hulme & Benkman 2002). Tolerance mechanisms do not prevent seed consumption but do reduce seed loss. The main tolerance strategy is the satiation and starvation of predators by means of large but irregular seed crops (Crawley & Long 1995).

In comparison to the above-mentioned plant traits, the relevance of seed size when accounting for differences in PSP remains much more elusive (Moles, Warton & Westoby 2003; Bonal, Muñoz & Díaz 2007). This ambiguity may be partly related to the particular way in which pre-dispersal predation often occurs. Most pre-dispersal predators are small, highly specialized insects, many of which develop inside the seed (Crawley 2000). Indeed, this particular form of endogenous seed consumption can give seed size an uncertain role in terms of likelihood of survival. Larger seeds are likely to suffer higher pre-dispersal predation than smaller seeds, because: (i) optimal foraging theory suggests the predator’s preference for larger seeds over smaller ones (Charnov 1976) and (ii) larger seeds may host both large and small insects (Mucunguzi 1995). Notwithstanding this, larger seeds may have a better chance of surviving predation because they can satiate the developing larvae before they reach the embryo, thus allowing the potential development of infested seeds into seedlings (Mack 1998). To some extent, small- and large-seeded plants could cope with the negative effects of pre-dispersal predation by means of different mechanisms (see Moles, Warton & Westoby 2003). However, the role of seed size per se in pre-dispersal predation can be difficult to separate from other plant traits closely related with this attribute, such as seed phenology or seed abundance. Larger seeds may be exposed to higher predation because they take longer to develop (Moles & Westoby 2004) or because the production of lower seed crops, as a result of a seed size abundance trade-off, may preclude the satiation of seed consumers (Bonal, Muñoz & Díaz 2007). Moreover, in plant communities that share common predators, predation risk of large- and small-seeded species may also depend on the size of the predators involved (Mendoza & Dirzo 2007).

The need then arises for an integrative approach to analyse and dissect the relative contribution of these factors (seed size, seed phenology and predator size) for interspecific differences in pre-dispersal predation. The main aim of this study was to investigate the interaction among seed phenology, seed size and predator size in the pre-dispersal predation of acorns in a mixed Mediterranean oak forest with two co-occurring oak species (the larger-seeded Quercus humilis and the smaller-seeded Quercus ilex), both depredated by two acorn weevils (the smaller Curculio glandium and the larger Curculio elephas). Our specific objectives were: (i) to examine any potential species-specific bias in acorn predation towards large-seeded oaks and to determine whether this was due to the deliberate selection of larger acorns by weevils, differences in acorn development phenology or differences in the ability of large and small acorns to host small and large weevils, (ii) to find out whether a more successful seed satiation of weevils by larger-seeded oaks could mitigate any potential species-specific bias in acorn predation and (iii) to assess whether small and large weevils differed in their ability to prey upon differently sized acorns. Finally, we discussed the results in light of how differences in seed size among oaks and in body size among weevils may promote the persistence of such a multi-host–predator system.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study site and species

This study was conducted in the Collserola Natural Park (Barcelona, Spain; 41°24′ N, 2°6′ E), a coastal massif with a Mediterranean-type climate. The park covers 8.5 km2, of which Q. ilex is present in 95% of the forested area and Q. humilis in 75%. The acorns of both the evergreen Q. ilex and the winter-deciduous Q. humilis mature within 1 year, but Q. humilis starts flowering c. 1 month earlier and produces larger acorns compared to Q. ilex (López & Sánchez 2004). We confirmed this difference in our study area after monitoring the size of acorns of the two species for 3 years (2005, 2006 and 2007). Mean acorn weight was significantly greater (anova, d.f. = 1, 362, F = 72.3, < 0.0001) in Q. humilis (1.1 ± 0.2 g) than in Q. ilex (0.5 ± 0.1 g), with minimum differences recorded in 2005 (Q. humilis = 1.0 ± 0.2 g and Q. ilex = 0.7 ± 0.1 g) and maximum differences in 2007 (Q. humilis = 1.1 ± 0.2 g and Q. ilex = 0.4 ± 0.1 g).

Two acorn weevil species have been observed to forage in these mixed-oak forests: C. elephas and C. glandium. Both larvae and adults are larger in C. elephas compared to C. glandium (head capsule size of larvae: C. elephas = 2.7 ± 0.1 mm and C. glandium = 2.2 ± 0.1 mm; R. Bonal & J. M. Espelta, unpublished data; for adults’ size see Fernández-Carrillo, Fernández-Carrillo & Alonso-Zarazaga 2002). After adults emerge, they climb the tree foliage and mate, and the females oviposit into the developing acorns that are still attached to the tree. Once they have been attacked, acorns drop prematurely (Bonal & Muñoz 2008). The larvae spend an average of 20 days feeding inside the acorn and then leave the acorn to bury for diapause (Bonal & Muñoz 2009).

Sampling design

We performed this study in a mixed-oak forest patch, where we selected 15 trees per species in July 2006. We conducted our study at a single site because preliminary long-term studies in the area have shown no influence of topography or forest structure on the extent of acorn predation by Curculio spp. in Q. ilex and Q. humilis trees (Espelta et al. 2008, 2009). Trees were randomly selected from among those with a similar d.b.h. in the two species (anova, d.f. = 1,28, F = 0.72, P = 0.41; Q. humilis = 17.3 ± 1.5 cm and Q. ilex = 15.8 ± 1.5 cm). Trees were tagged and four branches of similar size (c. 2–3 cm in diameter), all bearing incipient acorns, were randomly chosen for installing a seed trap on each branch. Each seed trap consisted of a mesh cage (30 × 50 cm) gently suspended surrounding the branch. These cages were open at the sides and top to allow the free movement of weevils while at the same time retaining all of the dropped acorns. The seed traps were visited every 15 days from 30 July to the end of acorn fall on 30 October. At each visit, dropped acorns were collected and classified as: (i) aborted (i.e. mal-developed or with some unidentifiable source of mortality not addressed in this study), (ii) infested by Curculio spp. (i.e. having the typical mark caused by the oviposition of Curculio spp., see Bonal & Muñoz 2007) and (iii) sound, mature acorns (i.e. naturally fallen sound acorns, present only at the end of the season from 30 September to 30 October). To establish the general pattern of acorn growth in the two species, we randomly collected and measured the volume of 10 sound acorns per tree (out of the seed traps) at each visit. Acorn volume was calculated by measuring length and width to the nearest 0.01 mm with a digital calliper.

At each visit, all acorns dropped into the seed traps were taken to the laboratory where their volume was measured. Infested acorns with the larvae still inside them (with oviposition scar and no larval exit hole) were kept separately, individually identified and placed in plastic vials to monitor larval emergence (Bonal & Muñoz 2009). The acorns were inspected daily, and the larvae leaving the acorn were collected, their head capsule measured as an estimate of body size (see Fox et al. 1996) and preserved in 100% ethanol. While adults of C. glandium and C. elephas can be easily identified by morphological characteristics, this is impossible to do so at the larval stage. Hence, larvae were identified to species level using DNA taxonomy. We extracted DNA from 118 larvae and sequenced a partial fragment (826 bp) of mitochondrial cytochrome oxidase subunit 1 (CO1) (for details of this methodology see: Pons et al. 2006; Ahrens, Monaghan & Vogler 2007). Species were identified against a set of reference sequences of European and American weevils obtained from adult individuals, which included sequences from C. elephas and C. glandium (Hughes & Vogler 2004).

Once larval emergence ceased, all infested acorns were dissected for inspection and classified as: (i) infested but only partly-depredated acorns: acorns with the embryo intact and retaining part of the cotyledons (if they have attained maturity, these acorns may well germinate, although their viability is lower, see Leiva & Fernández-Alés 2005) and (ii) depredated acorns: acorns with the embryo consumed, unable to germinate. In total, we dissected 274 acorns of Q. ilex and 616 of Q. humilis.

Acorn censuses and acorn classification in the laboratory enabled us to calculate the following variables per tree: total number of initial acorns produced, mean acorn volume of sound and infested acorns per sampling date, final number of sound acorns produced and final number of mature acorns produced (sound + infested but partly-depredated acorns). For the calculation of mature acorn production, we included only those infested but partly-depredated acorns dropped after 30 September, once mature sound acorns started to fall naturally. This was to ensure that these infested acorns were potentially germinable (for the effects of harvest date on acorn germinability, see Germaine & McPherson 1998). We also calculated, for each sampling date, the instant and cumulative rate of infestation and predation of acorns, and the proportion of depredated and infested acorns. Instant rates were calculated considering the number of acorns available to be infested (i.e. discounting the number of acorns dropped on previous sampling dates), while cumulative rates considered the total number of acorns initially produced.

The presence of adult C. glandium and C. elephas weevils in the area was monitored from 30 August onwards at every visit. Weevils were collected with an inverted umbrella held beneath the foliage while shaking the canopy of three Q. ilex and three Q. humilis trees surrounding those trees where acorn traps were installed.

Data analysis

Interspecific differences in the initial number of acorns produced, the final number of mature acorns and the final number of sound acorns were analysed by means of generalized linear models (GENMOD; SAS Institute, 1996), using a Poisson error distribution and a log link function. The effects of species, sampling date and their interaction on mean acorn volume were analysed by means of repeated-measures anova, while their effects on acorn infestation and acorn predation rates (instant and accumulated) and the proportion of depredated and infested acorns were analysed by means of generalized linear mixed models (SAS Institute, 1996) with a binomial error distribution and a logit link function. In these models, species, sampling date and their interaction were considered as fixed effects, whereas the factor ‘tree’ was included as a random factor, to consider the repeated measures nature of our analysis (Molenberghs & Verbeke 2005).

To explore the potential differences in the nutritional value of Q. ilex and Q. humilis acorns, a trait that could also cause a species-specific bias in the infestation of weevils, we conducted an ancova where the dependent variable was larval size and the independent variables were oak species and acorn size. This analysis was restricted to: (i) acorns infested by C. glandium (because of the low number of Q. ilex acorns infested by C. elephas, see Results), (ii) a common range of acorn sizes for Q. ilex and Q. humilis and (iii) to larvae grown ad libitum: i.e. larvae from acorns still containing traces of the endocarp, thus with their growth unconstrained by acorn size.

We used chi-squared tests to compare the presence of adults of C. elephas and C. glandium between sampling dates. The presence of larvae of both weevil species in acorns from both oak species on the different sampling dates was tested by means of log-linear models, including these three variables.

To analyse whether weevils deliberately select larger acorns, we compared the volume of sound and infested acorns from all sampling dates for the two oaks by means of a repeated-measures anova. In this analysis the sampling date was included as a fixed factor, because trees suffering from infestation may change between sampling dates, while the acorn condition (sound, infested) was treated as the within-effect factor to account for the association of both types of acorns within the same tree. This analysis was restricted to sampling dates when acorns of both species were infested (see Results).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The initial number of acorns produced did not differ between Q. ilex and Q. humilis (GENMOD, d.f. = 1,25, χ2 = 2.51, P = 0.11; Q. ilex = 33 ± 6 acorns and Q. humilis = 53 ± 11 acorns; values refer to the four sampled branches per tree). However, acorns of Q. ilex and Q. humilis differed in their growth pattern and in the final size attained (Table 1). Interspecific differences in acorn size were observed from the very first sampling date (30 July), yet differences increased progressively with a higher growth rate and a larger final acorn size for Q. humilis acorns in comparison to Q. ilex ones (Fig. 1a).

Table 1.   Results of the effects of species, sampling date and their interaction on acorn size, instant and cumulative rates of acorn infestation and acorn predation and the proportion of predated out of infested acorns. Effects on acorn size were analysed by means of repeated-measures anova while effects on the other variables were analysed by means of generalized linear mixed models (GLMM). For the GLMM, we indicate the value of the covariance parameter estimate ± SE
 Acorn sizeInfestation ratePredation rateInfestation/PredationCumulative infestationCumulative predation
d.f.FPd.f.FPd.f.FPd.f.FPd.f.FPd.f.FP
Species1,15014.7<0.00081,2923.7<0.00011,29.119.40.00011,21.34.50.04501, 2824.5<0.00011, 2921.0<0.0001
Date6,15072.4<0.00013,98116.7<0.00013,9891.2<0.00013,789.40.00803,100263.1<0.00013,100195.8<0.0001
Species × Date6,1505.0<0.00013,9816.0<0.00013,9819.7<0.00013,782.10.08123,10010.0<0.00013,10018.9<0.0001
Covariance parameter     1.33 ± 0.44  1.26 ± 0.42  0.38 ± 0.22  1.90 ± 0.60  1.47 ± 0.46
image

Figure 1.  Acorn development phenology (a) and acorn infestation and predation rates (b) in Quercus ilex and Quercus humilis. Infestation and predation rates are calculated taking into account the number of acorns available on every sampling date. Asterisks indicate significant differences between species per sampling date according to the least-squares means test. Mean ± SE values are represented. Sampling was conducted every 2 weeks between 30 July (30 J) and 30 October (30 O).

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Acorn infestation (acorns oviposited by Curculio sp. weevils) and acorn predation (acorns oviposited and depredated) differed significantly between the two oaks throughout the season (Table 1). As shown in Fig. 1b, infestation started 15 days earlier in Q. humilis (30 August) than in Q. ilex (15 September), and the former species suffered higher infestation and predation rates throughout the season. This resulted in a higher cumulative infestation and a higher cumulative predation in Q. humilis in comparison to Q. ilex (Table 1, Fig. 2). In spite of the consistency of the interspecific differences, the value of the covariance parameter for the subject level (tree) in Table 1 also suggests strong individual differences.

image

Figure 2.  Cumulative curves of acorn infestation and acorn predation in Quercus humilis (dots) and Quercus ilex (squares). Mean ± SE values are represented. Sampling was conducted every 2 weeks between 30 July (30 J) and 30 October (30 O).

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Interestingly, the proportion of acorns depredated out of those infested differed between species and throughout the season (Table 1): it was higher in the smaller-seeded Q. ilex (93.3 ± 2.0%) than in the larger-seeded Q. humilis (86.2 ± 2.6%) and it decreased in both species as acorn growth increased (15 September = 96.0 ± 1.7%, 30 September = 92.4 ± 1.8%, 15 October = 88.3 ± 2.1%, 30 October = 77.3 ± 4.4%). These results indicate the existence of interspecific differences in the potential satiation of weevil larvae by the acorns of the two oaks, as well as an increase in this seed-satiation effect as acorn growth increases.

An analysis of the size attained by weevil larvae in acorns of the two oaks revealed a significant and positive effect of acorn size on larval size (ancova, d.f. = 1,41, F = 29.2, P < 0.0001) but no effect of the oak species where they developed (d.f. = 1,41, F = 0.07, P = 0.80) or the interaction between oak species and acorn size (d.f. = 1,41, F = 0.06, P = 0.80). This suggests that interspecific differences in acorn infestation between the two oaks are not mediated by interspecific differences in the nutritional value of acorns.

Adult weevils of both C. glandium and C. elephas were collected in the study site from early September onwards. The former species was more abundant on all sampling dates (Fig. 3a), and the proportion of the two species did not change significantly throughout the season (χ2 test, d.f. = 3, χ2 = 1.2, P = 0.75). Notwithstanding the presence of adults of both Curculio species throughout the season, the molecular analysis of the larvae from the infested acorns revealed that C. glandium weevil infested acorns earlier than C. elephas (Fig. 3b,c). Concerning the two oaks species, infestation by both Curculio species occurred earlier in Q. humilis than in Q. ilex (log-linear model, interaction Quercus sp. × date effect: d.f. = 4, G2 = 9.9, P = 0.0422). Moreover, there were significant differences in the relative frequency of the two species of weevil larvae between oak species (log-linear model, interaction Curculio sp. × Quercus sp effect, d.f. = 1, G2 = 7.8, P = 0.0005). The presence of larvae of C. glandium was significantly higher in Q. ilex compared to Q. humilis; in fact, in the former more than 88% of the acorns were infested by C. glandium. The comparison of acorn growth phenology in Fig. 1a and the presence of Curculio sp. larvae in Fig. 3 shed light on the reasons for the earlier infestation of Q. humilis acorns and the almost exclusive presence of C. glandium in Q. ilex. Infestation of acorns by the smaller C. glandium occurred beyond a similar acorn size threshold in the two oaks (c. 0.4 cm3), but this threshold was reached almost 30 days earlier in Q. humilis (30 August) than in Q. ilex (30 September). This explains the higher infestation rates experienced by Q. humilis from 30 August to 30 September (see Fig. 1b). As for the larger C. elephas, this weevil infested almost exclusively acorns of Q. humilis because it requires a higher acorn volume threshold (above 0.6 cm3), rarely reached by Q. ilex acorns even at the end of the season (see Fig. 1a).

image

Figure 3.  Presence of adults of Curculio elephas and Curculio glandium in the study site (a), and presence of larvae of the two weevil species in Quercus humilis acorns (b) and in Q. ilex acorns (c). Numbers inside the columns indicate the number of adults sampled or the number of larvae identified by means of DNA taxonomy. Sampling was conducted every 2 weeks between 30 July (30 J) and 30 October (30 O). On 30 August (30A) we did not capture any C. glandium adults (Fig. 3a), although they were already present in the area as indicates the infestation by this weevil species of Q. humilis acorns on this date (Fig. 3b).

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The comparison of the volume of sound and infested acorns between sampling dates and between the two oaks revealed a preferential infestation of larger acorns at the beginning of acorn growth but not during the rest of the season (repeated-measures anova, acorn condition × sampling date effect, d.f. = 3,69, F = 7.2, P = 0.0002, Fig. 4). This indicates that, beyond the requirement of a minimum acorn size threshold for egg laying, there was no further selection for larger acorns. Furthermore, there was no bias in predation towards the larger acorns of Q. humilis, as suggested by the lack of significant differences in the interaction between acorn condition and oak species in this analysis (repeated-measures anova, d.f. = 1,69, F = 0.9, P = 0.333).

image

Figure 4.  Mean ± SE volume of sound (white dots) and infested (black dots) acorns for sampling date. Asterisks indicate significant differences between sound and infested acorns per sampling date according to the least-squares means test. Sampling was conducted every 2 weeks between 15 September (15 S) and 30 October (30 O).

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Despite the similar number of acorns initially produced by Q. humilis and Q. ilex, the higher infestation by Curculio spp. suffered by Q. humilis resulted in a lower final number of sound acorns in Q. humilis in comparison to Q. ilex (GENMOD, d.f. = 1, 25, χ2 = 6.85, P = 0.0089; Q. humilis = 3.7 ± 0.5, and Q. ilex = 7.5 ± 0.8; values refer to the four sampled branches per tree). Interspecific differences were still maintained after including infested but partly-depredated acorns as part of the final mature acorn crop produced (GENMOD, d.f. = 1, 25, χ2 = 4.61, P = 0.0271; Q. humilis = 5.8 ± 1.5, and Q. ilex = 9.5 ± 1.8; values refer to the four sampled branches per tree).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This study provides two main contributions to understanding the interaction between plants and granivorous insects. From the plant side, our results demonstrate that, while sometimes neglected, seed size matters, but so does seed phenology. Larger seeds may have a higher likelihood of predation because they can host both large and small insects, but also because they may reach earlier a minimum size threshold to be infested (see also Moles & Westoby 2004). Moreover, we show that predator satiation by larger seeds may barely offset the seed loss caused by a higher predation pressure. This warns about the overstatement of seed satiation as a mechanism to escape seed predation (see also Espelta et al. 2009). From the insect side, our results indicate that the smaller the insect, the higher its resource acquisition ability may be. Differences in acorn predation between small and large weevil species indicate that the former can infest seeds earlier and that it can infest both small and large seeds. Yet, above a minimum acorn size threshold weevils do not entirely follow an optimal seed size-based foraging strategy. All things considered, these results indicate that the complex interplay among seed size, seed phenology and predator size must be considered together to assess not only the ecological outcome of seed predation by insects (see also Pérez-Ramos et al. 2008), but also the potential existence of conflicting selective pressures on seed size (Gómez 2004) and predator size (Bonal & Muñoz 2009).

Seed size matters, but so does seed phenology

Although this was a single-year study, the higher acorn predation observed in Q. humilis in comparison to Q. ilex agrees with the results obtained in previous long-term monitoring surveys (Espelta et al. 2008, 2009). In these studies, we observed that both oaks benefited from their intra- and interspecific masting behaviour to reduce acorn predation, but that Q. humilis systematically suffered from higher predation than Q. ilex. Such a size-biased predation risk had been previously reported for larger-seeded oaks (Bonal, Muñoz & Díaz 2007; Xiao, Harris & Zhang 2007), but the causes had not been clearly elucidated. According to our results, acorns of Q. ilex and Q. humilis were equally infested beyond a similar size threshold and no differences in larvae growth were observed between acorns of the two species (i.e. potential absence of nutritional differences among oaks). This suggests that differences in predation are mostly due to differences in acorn phenology and acorn size. However, the strong individual variability observed suggests that other factors, not addressed in this study, may also determine individual differences in seed predation (e.g. spatial and temporal effects in Kolb, Ehrlén & Eriksson 2007).

Earlier acorn growth in Q. humilis dramatically accounted for much of the higher predation suffered by this species in comparison to Q. ilex (Fig. 2). The advantage of producing seeds off-peak (earlier or later) to reduce seed predation has been mostly discussed in light of the probable lower presence of herbivores at this time (Elzinga et al. 2007). Such a slight decrease in the presence of Curculio spp. at the end of the season would benefit Q. ilex, as it later reaches an acorn size threshold suitable for infestation. Yet, Q. ilex may also benefit from the partial satiation of weevils by the earlier infestation of Q. humilis acorns. On the average, an adult weevil female lives 28 days and lays 28 eggs (Menu & Debouzie 1993). As they start ovipositing as soon as acorns are large enough to ensure larval development (Bonal & Muñoz 2008), earlier-emerged females will have already laid part of their eggs in Q. humilis once infestation in Q. ilex acorns starts. To our present knowledge, this is the first time that such a potential ‘free-rider’ effect (i.e. a species benefiting from a reduced seed predation on account of the earlier infestation of a congeneric one) is suggested. Certainly, further research is necessary to assess whether the benefits of a smaller seed size and a later phenology in Q. ilex are available in most years, and whether these benefits might be altered by other processes (e.g. acorn dispersal, post-dispersal predation).

Differences in acorn size not only accounted for interspecific differences in infestation risk but also for differences in the possibility to survive infestation (seed satiation). As thoroughly reported (for oaks, see Xiao, Harris & Zhang 2007; for other species, Rosenthal & Kotanen 1994; Mack 1998), larger acorns of Q. humilis could better satiate larvae than smaller acorns of Q. ilex, even though the former species suffered higher infestation by the larger weevil C. elephas. Nevertheless, the fact that a higher seed satiation potential could not offset interspecific differences in the final number of mature acorns warns about the overstatement of the benefits of a larger seed size to escape predation by insects (see also Espelta et al. 2009).

The smaller the insect, the higher its resource acquisition ability may be

Different studies have reported a close relationship among seed size, larvae size and, finally, adult insect size (Fox et al. 1996). Therefore, as oviposited acorns stop growing and are prematurely abscised, weevils have to infest acorns with a minimum size to guarantee larval feeding and survival (Bonal & Muñoz 2008). This consistently explains the earlier oviposition phenology in the smaller-sized C. glandium in comparison to C. elephas and the need for larger acorns by the latter species. However, beyond a minimum acorn size threshold, our results suggest no further positive selection of larger acorns by weevils (for similar results, see Desouhant 1998). Adult weevil females have a narrow temporal window in which to oviposit: namely, after acorns reach a minimum size but before superparasitism (i.e. different females laying in the same acorn) occurs (Jimenez et al. 2005). Furthermore, as the season progresses, the number of available acorns decreases due to the premature abscission of infested acorns and the fall of sound mature ones (Bonal & Muñoz 2008). This lack of seed size effects for weevil predation (beyond a minimum size threshold) suggests that granivorous insects may not totally follow a seed size-based optimal foraging strategy, as has often been reported for vertebrate predators (Hulme 1998; Gómez 2003; Gómez, García & Zamora 2003; Pons & Pausas 2007).

Perspectives

Once the disadvantages of larger-seeded oaks and larger weevil species have been established, a question arises: why are these species not excluded? Indeed, other size-based processes might compensate for the above-mentioned disadvantages. The higher predation suffered by Q. humilis can be offset by differences during seedling establishment: i.e. seedlings established from less numerous but larger acorns of Q. humilis may outperform seedlings of Q. ilex especially under harsh environmental conditions (e.g. shade in Espelta et al. 2005; see also Quero et al. 2006). This suggests that a predation versus competition trade-off might assist the co-existence of these two oaks, at least during recruitment (see also Gómez 2004). Concerning the persistence of the larger weevil species, the positive relationship among body size and some fitness traits (fecundity in Desouhant et al. 2000; survival of larvae in Bonal & Muñoz 2009), might partly compensate its lower foraging ability. Clearly, the assessment of other size-based processes, not addressed in this study, and a more accurate analysis of within-species variability would be necessary to elucidate whether acorn size and weevil size are subjected to conflicting pressures.

This study shows that seed phenology and seed size can reduce seed predation risk for some species while making others more susceptible to it, i.e. species producing later and smaller seeds may be favoured on account of the earlier predation of large-seeded companion species. To what extent this pattern occurs in other plant communities and whether the phenological sequence of acorn growth and weevil infestation observed here (larger seeds develop earlier, larger insects infest later) promote the persistence of such a multi-host–predator system are two exciting questions to be further investigated. At the same time, it will be necessary to assess whether these interactions may be disrupted by the phenological changes induced by new climatic scenarios. Recent studies have reported a reduction in acorn crop size in Mediterranean oak forests subjected to increasing drought (Ogaya & Peñuelas 2007) as well as a shift towards an earlier ripening of acorns (Peñuelas, Filella & Comas 2002). Whether these changes may alter the strength of the interaction between plants and granivorous insects deserves further attention.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We would like to thank Helena Barril, Lidia Guitart and Xavier Arnan for their field and laboratory assistance. We are also indebted to Dr Alfried P. Vogler, who allowed us to conduct the molecular larval identification on his laboratory facilities at The Natural History Museum, London. Two anonymous referees provided valuable comments on an earlier draft of this manuscript. This research has been funded by the projects, MCIIN (CGL2008-04847-C02-02) and Consolider-Ingenio Montes (CSD2008-00040), and the Consorci del Parc de Collserola.

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  6. Discussion
  7. Acknowledgements
  8. References
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