As for our third question regarding the effect of species removal on plant reproductive success, the loss of the migratory hummingbird is associated with negative effects in California and positive effects in Mexico . In the case of California, Ribes sanguineum shows decreased fruit set after the loss of the migratory hummingbird , and all three plant species show slightly decreased fruit weight . Castilleja affinis shows a decrease in fruit length and width with loss of the migrant hummingbird . By contrast, in Mexico the number of seeds per fruit increases with the loss of the migratory species for three of the four plant species sampled . In addition, two of the species show an increase in fruit length and fruit width .Our results show that the foraging niches and functional roles of individual hummingbird species are dynamic and shift across their distribution areas. In particular, in the case of S. rufus its role changes from generalist to highly specialist in the community, and these niche shifts have a direct effect on its effectiveness as a pollinator. Moreover, our results prove that the temporary local removal of a species can lead to important changes in the functional roles covered by the remaining species, 10 liter drainage pot and that these changes have an effect on the functions they perform. Here, we see the greatest changes in the niches occupied by one hummingbird species in Mexico and one in California .
In both cases, the species expand their niches and become more important in the community with the loss of the migrant from the community. However, these changes entail different consequences across the biodiversity gradient. In Mexico, the larger diversity of hummingbird species allows for another species to take over the role of the lost migrant, maintaining and even improving on the function performed by the latter. Conversely, in California, where hummingbird species diversity is lower, the role of the migratory species is not fully covered in its absence, leading to a reduced function. Previous experimental research has suggested that species’ functional roles shift in response to changes in community composition with differing consequences for the functions performed. While Brosi & Briggs found a negative effect of the loss of an abundant bumblebee for the reproductive success of Delphinium barbeyi , Hallett et al. found that the exclusion of bumblebees did not compromise the success of Asclepias verticillate . In this second case, the role of the lost species was taken over by another species . However, these studies, although highly valuable, were both carried out at small spatial scales and for relatively short periods of time, and focused on the reproductive success of just one species of plant. By contrast, our use of migratory species as a proxy for species loss allows us to evaluate the consequences of whole-landscape removals of the same species on natural communities along latitudinal gradients and to focus on the consequences for a larger subset of the plant species in the community.
Of course, the continental scale of our approach and the fact that we have data for just 1 year also present some caveats, such as the confounding effect of latitude and diversity. By using a landscape-level natural removal of a species, we are able to show how species loss has large negative effects on some plant species, no effect on others, and in some cases produces effects that are over-compensated by changes in the roles of remaining species. Although our systems is not exactly a replica of a species extinction, since the communities we study have evolved with the presence of this migratory species, it clearly shows that understanding the consequences of species loss for ecosystem persistence requires of a community-level approach that focuses on the combined responses of multiple species and that takes into account the possible behavioural changes of the remaining species. Our results provide evidence of the role of biodiversity as insurance against species loss [29]. As the migratory species disappears, we find that in the more diverse community the functions it performs are covered by other species that compensate for the loss and even improve the function of the lost species, thus ensuring the stability of the system. However, in the less diverse community, lower hummingbird diversity precludes the function of the migratory species from being covered by other hummingbird species and leads to a greater than 10% decrease in the reproductive success of the migrant’s preferred plant species. It is important to note that although the species Hylocharis leucotis seems to takeover the role as pollinator for most plant species visited by S. rufus in its absence, our analyses of the motif signatures of both species show some disparities suggesting that the resident species is not fully able to cover the role of the migrant.
Nevertheless, the functional consequences of changing the indirect interactions captured by motif analyses are still far from being fully understood. Insect pollinators, present during both periods, may also be important pollinators in these systems, yet their activity is apparently not able to compensate for the loss of this one species from our observations. However, including insect species would have allowed us to evaluate the structure of the whole network of interactions involving plant species which could potentially reveal interesting results. We also show how this species’s foraging niche can dramatically change along its distribution range. In particular, we find that S. rufus behaves as a more generalist species at its wintering and breeding areas, while it becomes a specialist during part of its migratory journey. This difference has a consequence for the role the species occupies in the community, which becomes more important in the area in which it behaves as a specialist and apparently more efficient pollinator. This result has implications for trying to determine the resilience of natural communities to species loss. Early efforts at doing so assumed that species loss meant interactions loss, allowing no restructuring or rewiring of interactions . More recent efforts have tried to take into account the ability of natural systems to restructure through species role changes by allowing a certain level of interaction rewiring . Although we are still far from understanding what drives changes in species behaviours and what the consequences of these changes are, our study clearly shows that interaction rewiring may be common and is important for both sides of bipartite interactions like plant–pollinator networks. The existence of interaction rewiring might be more common in systems like ours adapted to annual migration processes, yet the frequency of this phenomenon across different ecosystems is not yet clear. Global change impacts are particularly pressing in the case of migratory species, which are forced to shift their migratory behaviours in response to changes in the suitability of their breeding and wintering habitats. Much global change research has been devoted to studying the changes to the migratory routes, departure or arrival dates of migratory species, yetless attention has been given to the functional impacts that these changes could have within the natural communities that support them. Indeed, migratory species transport nutrients and energy as well as other organisms between distant locations, thus coupling ecological communities throughout their migratory routes. Studies focusing on the interactions between migrant and resident species have shown that migrants can alter food web topologies, and the structure and dynamics of natural communities. Migrants thus have the potential to affect ecosystem functioning across the different resident communities they connect in their journeys, and understanding their impacts requires of integrative studies linking bio-geography to community ecology among other disciplines. In the case of hummingbirds in particular, migrant species are key players that increase plant–hummingbird network cohesiveness by interacting with a diverse set of plant species. They are present in fruits, bark, leaves, 25 liter pot and seeds of many plants, and are postulated to play protective roles. These phenolic compounds are also recognized as useful agents for human health . PAs consist of Xavan-3-ol units that are synthesized via the pathway leading to various phenylpropanoid compounds such as Xavonols and anthocyanins . Catalytic and regulatory mechanisms of phenylpropanoid metabolism have been elucidated well and a number of molecular components have been identified . Notably, two Xavonoid reductases, leucoanthocyanidin reductase and anthocyanidin reductase , have been shown to compete with the biosynthesis of anthocyanins, catalyzing steps committed for PA biosynthesis.
Tanner et al. identified LAR, which catalyzes conversion of the immediate precursors of anthocyanidins to one of the PA subunits, 2,3-trans-Xavan 3-ols [e.g., -catechin], from the legume Desmodium uncinatum. Xie et al. demonstrated that anthocyanidins are common precursors to anthocyanins and PAs by identifying the BAN gene product as ANR, which converts anthocyanidins to the other PA subunits, 2,3-cisXavan-3-ols [e.g., -epicatechin], in Arabidopsis thaliana and Medicago truncatula. In addition to the biosynthetic enzymes, MYB transcription factors have been shown to regulate PA accumulation in several species, such as A. thaliana and grapes . One of the outstanding questions regarding the mechanism of PA metabolism is if and how Xavan-3-ols are sorted from the cytoplasm to the vacuole, where they are postulated to be polymerized. Recently, several candidates involved in this process have been identified. One of them is a glucosyltransferase , UGT72L1, from M. truncatula . Transcriptional profiling led to identification of the UGT72L1 gene, whose expression correlated well with massive accumulation of PAs and the presence of a low but significant amount of -epicatechin glucoside in the seed coat of M. truncatula. A further biochemical study established the epicatechin 3 -O-GlcT activity of the UGT72L1 protein. Another component is a multidrug and toxic compound extrusion-type transporter, TRANSPARENT TESTA 12 , from A. thaliana. A genetic study showed that TT12 is necessary for PA accumulation in seeds . A fusion of TT12 and green Xuorescent protein was targeted to tonoplast in vivo, and yeast microsomes producing the TT12 protein were shown to have a cyanidin-3-O-glucoside/H+ antiporter activity in vitro . Direct evidence for transport of Xavan-3-O-glucosides through TT12 into the vacuole has not been provided yet. Nonetheless, these findings have led to a model for the critical step of PA biosynthesis, i.e., glycosylation and transport of Xavan-3-ols from the cytoplasm to the vacuole where they are probably deglycosylated and polymerized .A wide variety of plants is rich in PAs. However, only a handful of species has been used for biochemical and functional studies of these polyphenolic compounds. Among under-examined species is persimmon . Although it has not been mentioned in most review articles on PAs , D. kaki accumulates a large amount of high molecular weight PAs in leaves and fruits . In Japan, this species provided the fifth most consumed fruit in 1996, and its immature fruits have been the source of kaki-shibu, the material rich in soluble PAs utilized in various industrial applications . Persimmon cultivars can be divided into astringent – and non-astringent -types based on the amount of soluble PAs in mature fruits, which cause astringency in the mouth upon consumption. Soluble PAs in A-type fruits can be removed by ethanol treatment; this produces acetaldehyde, which in turn induces PA polymerization . Insolubilization of PAs during A. thaliana seed development was also shown to be caused by their oxidative polymerization . Hence, PA solubility in persimmon fruits may be negatively correlated with oxidation level as well as the degree of polymerization. Fruits of both A- and NA-types are rich in the soluble PAs in their early developmental stages. The NA-type loses its astringency during the development on the tree and becomes non-astringent with firm Xesh. By contrast, the A-type fruit needs to be kept on the tree until it becomes over-ripe and extremely soft, or has to be subjected to pre- or post-harvest treatments, such as that with ethanol as described above, for removal of soluble PAs before human consumption . A limited number of works has described the composition and structure of PAs in A-type fruits . The presence of soluble 2,3-cis– and –transXavan-3-ols in both A- and NA-type D. kaki fruits was also reported . In addition, accumulation of transcripts encoding putative homologs to Xavonoid biosynthetic proteins was reported in PA-rich persimmon fruits . Overall, however, there has been no systematic study to clearly deWne compositions of PAs and other phenylpropanoid components of persimmon fruits. Furthermore, the molecular mechanism of PA accumulation in this non-model species remains largely unexplored. This situation may be mainly due to prolonged life cycle and genetic complexity of this hexaploid species.