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- Materials and methods
- Supporting Information
Global climate change is now taking place at an unprecedented rate (Parmesan & Yohe 2003; Root et al. 2003; Schröter et al. 2005; IPCC 2007). The biological effects of this global change have already been documented by detailed studies of a wide variety of organisms; many investigations reported a shift in phenology as a response to climate change (e.g. Fitter & Fitter 2002; Parmesan 2006; Post et al. 2008; Végvári et al. 2010).
Shifting vegetation phenology is likely to be the main mediator of climate change for animals (Bonan 2008). Consequently, understanding the responses of primary producers to climate change is particularly important for understanding its effects on all trophic levels. On the other hand, plants are also affected by other organisms in interactions such as herbivory, parasitism and pollination. In the case of herbivory and parasitism, plants may benefit from shifting their phenology if the result is an ecological mismatch that reduces damage caused by parasites or herbivores. Conversely, any phenological mismatch between pollinators and flowering plants may significantly decrease pollination efficiency and thus reduce the reproductive success of plants (Fitter & Fitter 2002; Hegland et al. 2009; Bartomeus et al. 2011; Rafferty & Ives 2011). Indeed, some studies partially attribute the recent pollination crises – the serious decline of some insect-pollinated plants and their pollinators – to climate change (Dixon 2009; Anderson et al. 2011; Bartomeus et al. 2011). Consequently, plant–pollinator relationships should be considered in studies of plant responses to environmental change.
In addition to ecological interactions, at least three other factors are likely to explain interspecific variation in the reactions of plants to climate change. First, although most ecosystems are experiencing the effects of increasing temperatures (Walther et al. 2002), the amplitude of temperature change varies geographically (IPCC 2007). Biological responses to changing environmental conditions are therefore unlikely to be uniform on geographical scales, implying that species inhabiting different environments will show different phenological responses (Menzel et al. 2006; Askeyev et al. 2010). For example, spring phases have been advanced in western and central Europe but delayed in eastern Europe (Ahas et al. 2002). Hence, to get a better understanding of climate change, we need detailed investigations of plant phenological alteration from regions of the world that are currently understudied, such as central Europe.
Second, changes in climatic conditions are not always identical at different times of the year, even at the same location (Schwartz, Ahas & Aasa 2006; Walther 2010). Therefore, plants whose active periods occur in different times of year are expected to show contrasting climatic responses. Seasonal differences in plant reactions to warming have been observed both in historical investigations of phenology (Fitter & Fitter 2002; Sparks & Menzel 2002; Walther 2004) and in experimental warming studies (Price & Waser 1998; Dunne, Harte & Taylor 2003; Sherry et al. 2007). One would expect that plants flowering early in spring will respond more readily to global change (Fitter & Fitter 2002; Sherry et al. 2007), because they are already adapted to more variable spring weather. This effect may be strengthened by the greater degree of warming during winter and spring compared with other parts of the year (Schwartz, Ahas & Aasa 2006).
Third, the ability of an organism to follow shifting environmental conditions is thought to depend on its life-history traits. A survey of British plants showed that annuals were more likely than perennials to advance flowering (Fitter & Fitter 2002). A possible explanation for this observation is that species with shorter life spans have shorter generation times and hence can adapt more quickly to changing conditions (e.g. Baker 1974; Jump & Peñuelas 2005). On the other hand, longer-lived plant species might show a greater degree of phenotypic plasticity that could, in principle, allow them to track environmental conditions associated with climate change more accurately compared with shorter-lived species (e.g. Hoffmann & Sgrò 2011). In summary, pollination mode, geographical distribution, timing of activities within the year and life span are likely to influence phenological responsiveness in plants.
Terrestrial European orchids are ideal for studying the effects of pollination mode on flowering phenology, because, although they are mainly self-compatible (Neiland & Wilcock 1999), they maintain diverse pollination modes: many of them are self-pollinating (including obligate and facultative inbreeders), others reward pollinators with nectar and approximately one-third of the species use various forms of floral deception (Dafni 1984; Jersáková, Johnson & Kindlmann 2006). The flowers of deceptive orchids mimic food or receptive females, luring insects to transfer pollen without substantially rewarding them. Pollination of deceptive plants differs from that of nectar-rewarding ones because their pollination is accomplished only by visits from inexperienced insects that have not yet learnt to avoid non-rewarding flowers (Schiestl 2005). Learning takes time; therefore, in deceptive orchids, the reproductive success of early inflorescences tends to be higher (Jacquemyn et al. 2002), and the earliest flowers of the inflorescence have a better chance of being pollinated (Vallius 2000; Jacquemyn et al. 2002). A further reason for investigating climatic responsiveness in orchids is that many species of this charismatic group are of key conservation importance (Jacquemyn et al. 2005; Kull & Hutchings 2006; Swarts & Dixon 2009). Finally, orchids have long been popular among both professional and amateur botanists, leading to the accumulation of extensive long-term herbarium collections. Such collections are especially important in analysing phenological responses of plants (Miller-Rushing et al. 2006; Primack & Miller-Rushing 2009; Robbirt et al. 2011; Panchen et al. 2012). The Herbarium Database of Hungarian Orchids has recently been compiled from all publicly accessible Hungarian herbaria (Molnár V. et al. 2012). The data set analysed in this paper is based on this large data base. It contains flowering data for 41 native orchid species, which represent 66% of the countries' current orchid flora (only very rare taxa are missing; Molnár V. 2011). Our data set spans more than 170 years and covers the entire present day territory of Hungary.
In this study, we utilize this large Hungarian data set to study the phenological responsiveness of orchids. Specifically, we focus on the following questions. First, given the overarching importance of ecological interactions, how does pollination mode influence the response of plants to climate change? Second, do characters related to the spatial distribution of species affect phenological response? Biogeographical distribution type (e.g. Mediterranean vs. non-Mediterranean) and the altitude of the preferred habitat can indicate complex life-history adaptations to contrasting climatic conditions. Therefore, different phenological response to global change by plants with different distribution type and altitude is expected. Third, do early flowering orchids show a stronger phenological response to climate change, mirroring what has already been demonstrated for a wide taxonomic range of flowering plants (Fitter & Fitter 2002; Sherry et al. 2007)? Fourth, how does life span predict the magnitude of phenological responses in plants? A larger potential to adapt to climate change has been postulated for short-lived plants, reflecting their faster reproductive cycle (Jump & Peñuelas 2005). Are short-lived orchids more responsive phenologically? Finally, we were also interested in the way phylogeny affects changes in flowering time because other studies (e.g. Willis et al. 2008; Davis et al. 2010) have found phylogenetic relatedness to be a crucially important predictor of responsiveness to changing climate.
- Top of page
- Materials and methods
- Supporting Information
Our study yielded three main results. First, the majority of orchid taxa analysed advanced their flowering date over the studied time period. Second, pollination mode and life span emerged as factors strongly and consistently related to the degree of advancement in flowering in all analyses, regardless of the method of measuring phenological change (Table 3). Flowering time was a strong predictor of phenological response only in the analyses considering the correlation between years and flowering time (temporal trend). Additionally, biogeographical distribution type was found to be only moderately important in predicting shifts of flowering date. Third, phylogenetic relatedness exerted little constraint in all models fitted on both trends and change of flowering dates.
Interestingly, self-pollinating orchids, which are unconstrained by pollinators, have advanced their flowering date most strongly, whereas the degree of advancement in insect-pollinated taxa depended on the specific nature of their entomophily. Deceptive species showed almost as much advancement as autogamous species, whereas nectar-rewarding orchids did not respond to increasing spring temperatures. This is consistent with the hypothesis outlined in the introduction. Nectar-rewarding species are likely to be constrained in responding to climate change due to their extensive interactions with pollinators (Hegland et al. 2009), if pollinators advanced more slowly than orchids would. Unfortunately, no data are available to support this idea. As for deceptive species, they compete intensively for naïve pollinators (Schiestl 2005); therefore, they are expected to be very sensitive to environmental variations in order to successfully synchronize their flowering before the first appearance of their pollinators even in years when spring starts very early. Indeed, they flower earlier than nectar-rewarding orchids (Internicola, Bernasconi & Gigord 2008; Internicola & Harder 2012; Pellissier et al. 2010). Accordingly, mean flowering date of deceptive orchids in our sample is 30 May, while it is 15 June for nectar-rewarding species. (note that the effect of pollination mode on phenotypic response was detected after controlling for all other variables.) As a result, deceptive orchids are likely to follow climate change more easily than nectar-rewarding species. Nevertheless, more investigations are needed to clarify the role of pollination modes in explaining phenological shifts.
Life span was found to be another important predictor of climatic responsiveness. Contrary to our expectations, long-lived species had more advanced flowering dates than short-lived species. Although this result contradicts the prediction that shorter life span might strengthen selection for the advancement of flowering (Fitter & Fitter 2002; Jump & Peñuelas 2005), it was obtained consistently from our various analyses, suggesting that phenotypic plasticity in long-lived orchids is a stronger driver of climatic responsiveness than evolutionary adaptation. Together with a similar finding by Gienapp, Leimu & Merilä (2007), this observation indicates the important role of phenotypic plasticity in shaping climatic responses over relatively short time frames. In a way, this is not surprising, as long-lived organisms are predicted to meet more diverse environmental conditions during their life than short-lived ones. Therefore, they may be better prepared to flexibly respond to environmental changes. Note, however, that presently, we possess data on the life span of orchids but none on their relative levels of phenotypic plasticity. Researchers have just started to characterize epigenetic variation in European orchids (Paun et al. 2010, 2011). Since epigenetic change may underpin phenotypic plasticity, it may be crucially important in adaptation to changing environments.
Throughout various analyses, we found that the strength of phylogenetic signal did not differ markedly from zero for both measures of the advancement of flowering dates. This result parallels the results of a previous investigation showing that the advancement of spring migration among a large selection of bird species did not reflect phylogenetic signal (Végvári et al. 2010). The fact that we did not find phylogenetic signals in our response variables implies that sensitivity to climatic effects in Hungarian orchids can be treated as a species-specific response, free of phylogenetic inertia. Although certain life-history traits (flowering time, pollination mode, life span; see Table 1) did show a significant phylogenetic signal individually, they were not correlated and hence can be viewed as being independent of each other. Therefore, the apparently strong and opposing effects of life-history variables in closely related taxa can lower the similarity of related species and hence decrease the strength of phylogenetic signal in phenological response. The lack of overall phylogenetic inertia contrasts with the conclusions of Willis et al. (2008) and Davis et al. (2010), who studied the climate change-driven species loss within given territories. The reason for this discrepancy may lie in the contrasting taxonomic coverage of the studies: the above-mentioned works included a wide range of plant species sampled from several taxonomic families, whereas the species included in this study are less taxonomically diverse. Taking this question one step further, we can ask, might phylogenetic signals only influence flowering phenology at higher taxonomic levels (i.e. among families)? This question clearly warrants further investigation.
Our analyses seem to suggest that flowering time is not a robust predictor of climatic response in orchids, as it proved to be important only in shaping the temporal trend in flowering date of the studied orchids, but it had no strong effect on the shift in flowering date after 1960 (Table 3). This is especially interesting because in other studies (e.g. Sparks, Jeffree & Jeffree 2000; Cleland et al. 2007), flowering time was found to be an important factor influencing phenological response. However, we feel that this discrepancy might be caused by the relatively small number of taxa in our study. Clearly, more research is needed to verify the importance of flowering time in predicting phenological response in orchids.
Biogeography was found to be moderately related to the advancement of flower production in orchids; species with a Mediterranean distribution tended to accelerate flowering more than non-Mediterranean species. The reason for this difference is currently unclear, but a Mediterranean type of distribution might indicate a life-history adaptation that benefits from the recent climate change through, for example, photoperiod, temperature cues, vernalization or precipitation (Forrest & Miller-Rushing 2010).
Our analyses revealed no influence of altitudinal distribution on the advancement of flowering, implying that this life-history component has a minor impact on response to climate change in the orchids investigated here. This is interesting because one would expect species at higher altitudes to show stronger phenological advancements through time because temperatures are increasing at a faster rate at higher altitudes (Lenoir et al. 2008). Nevertheless, we do not claim that altitude may have no importance in general, given that our records represent a geographical region where the altitudinal range is relatively small (76–1014 m a.s.l.).
Although our study may have been adversely affected by varying sampling frequency, the two measures of historical phenological responses used here yielded consistent results. As the cumulative temperature between January and May showed a marked increase in Hungary during the study period, our findings indicate that temperature may (e.g. through vernalization) play an important, but certainly not exclusive, role in the advancement of flowering time in orchids (cf. Miller-Rushing & Primack 2008; Primack & Miller-Rushing 2011; Robbirt et al. 2011).
The differences in the relative importance of predicting factors using the two measures of phenological change could stem from the fact that these two measures might be affected differently by variation in sampling intensity through time. Although records for most species originate from relatively long periods (Table S2 in Supporting Information), there were year-to-year variations in sampling intensity and some gaps in the recording activity. Considering these potential problems, we believe that comparing flowering times between the first and second parts of the sampling period is less affected by sampling bias and hence provides a more reliable estimate of the advancement of flowering date. In addition, our measure of temporal trend is based on the ranks of flowering time, and hence, it eliminates some of the variation. In contrast, the shift in mean flowering date uses the actual number of days of change and might be a more sensitive measure of phenological response.
In summary, we have demonstrated in a diverse set of orchid species that changes in flowering phenology through time (which is associated with increased temperatures in the study area) seem to be affected most strongly by pollination mode and life span. According to our findings, deceptive or autogamous, long-lived, or early flowering, terrestrial orchids with mainly Mediterranean distributions (in our data set this category is exemplified by O. simia or A. pyramidalis) follow the changing climate more closely, at least in Hungary. Meanwhile, their later flowering, nectar-rewarding or short-lived counterparts with non-Mediterranean distribution type (as exemplified by Dactylorhiza viridis) do not or less markedly respond to these changes.