Mutualistic interactions between species are essential for the survival and persistence of many native plants; however, their consideration in restoration efforts is often overlooked (Handel 1997). These interactions provide vital services to wildlife such as the basics: food, shelter, and/or favorable microsites (Handel 1997; Maestre et al. 2001). Unfortunately, many plant populations may not become self-perpetuating without their coevolved (or fortuitous) mutualists. Since repeated reintroductions of plant species are neither cost effective nor successionally progressive, mutualists must be considered to enhance the success of any plant restoration project.
Most degraded environments suffer some loss of these important mutualists due to various anthropogenic disturbances such as habitat fragmentation, erosion, soil compaction, pollution, pesticide/herbicide use, competition with invasive species, destruction of nesting habitat, and the loss of suitable host plants (Handel 1997; Cane & Tepedino 2001; Hobbs 2002; Ness and Bronstein, 2004). Approximately 90% of all plants exclusively depend upon pollination by birds, bats, insects or other animals. While several different pollinators may service some of these plants, some degree of host specificity is usually required for effective pollination rates (Handel 1997). Although animal-mediated seed dispersal is thought to be a more diffuse mutualism than pollination (Wheelwright & Orians 1982), it is still an valuable strategy for plants that can reduce competition with the maternal plant, reduce density dependent mortality, reduce seed predation, protect seeds from unfavorable environmental conditions (i.e. fire) and/or be preferentially directed to favorable microsites (Beattie 1985; Boyd 2001; Wenny 2001). Finally, endophytic fungi are abundant in all plants (Arnold et al. 2000; Schulthess & Faeth 1998) and the type of symbiosis varies from antagonistic to mutualistic (Faeth 2002; Hayes & Faeth 2002). Although these fungal symbionts can have significant effects on plant fitness (Clay 1998; Faeth 2004; Arnold et al 2003; Jumpponen & Trappe 1998), they have been largely ignored or excluded (due to concerns about livestock poisoning via endophyte-produced alkaloids) in restoration efforts (Faeth et al. submitted manuscript).
Pollinators
Animal-pollinated plants without available pollinators are termed the “living dead” (sensu Janzen 1986) and their incorporation into restoration programs is futile since they will be unable establish a self-perpetuating population (Handel 1997). Land managers have three basic options to remedy this problem (although not mutually exclusive): 1) Attract pollinators to the site 2) Reduce mortality of native pollinators 3) Reintroduce native pollinators to the site (Handel 1997; Kearms et al. 1998).
Establishing corridors between patches
Creating linkage between habitat patches is always a goal of any restoration effort. While this connectivity may benefit plants by promoting higher levels of gene flow and reducing the probability of local extinctions (Wright 1943; Gilpin 1987; Lande 1988), it may also provide a route with stopover points for migratory pollinators (Dobson et al. 1999; Whisenant 1999). Although there has been controversy regarding the effective size of these linkages, current recommendations suggest that the width of these corridors should be greater than one home range (Dobson et al. 1999; Nabhan 2001). In addition the shape and size of habitat patches across the landscape heavily influences the direction and rate of succession. Further, the availability of sequentially flowering host plants along the pollinator migration route will also determine effectiveness of these linkages (Nabhan 2001). Often the installation of many small clusters of plants may provide a more continuous source of pollen and nectar than a few large stands of plants (Whisenant 1999; McDonald 2000). For example, Nabhan (2001) found that both migratory pollinators and other invertebrate pollinators in fragmented habitats benefited from this type of linkage. For this project, he utilized private farmland and other disturbed areas to plant small clusters of wildflowers and artificial nests to act as a corridor between regional reserve networks.
Shelter
In degraded landscapes, many pollinators suffer from the lack of available shelter or nesting areas. This is particularly a problem in sites that have heavily engineered/compacted soils or have been cleared of dead trees and decomposing wood. For example, Handel (1997) suggests the use of constructed sandy soil plots to provide habitat for ground nesting pollinators. Urban structures can also be exploited as potential pollinator habitat. For example, sand and gravel levees have been shown to provide suitable habitat for ground nesting bees (Kearns et al. 1998). Similarly, artificial soil beds are employed to attract alkali bees, which are effective pollinators of many crop plants as well as reintroduced natives (Buchmann & Nabhan 1997). For wood colonizing bees, woodpiles should be left on the site and perhaps supplemented with wood nesting boxes (Brown 2002)
Pesticide/herbicide use
The recent dramatic decline of honeybees and native pollinators has been at least partially attributed to the overuse of broad-spectrum pesticides and herbicides. Native pollinators suffer the greatest decline in areas in the proximity of application. In fact, hummingbirds, bats, bees, and many butterfly declines have all been associated with pesticide/herbicide use. Pesticide contamination can taint the available nectar sources whereas herbicide can reduce the availability of nectar all together by killing the nectar-producing plants (Kearms et al. 1998). Therefore, the use of these toxic chemical near natural remnants or restoration sites should be limited an/or less harmful alternative should be employed when available.
Reintroduction
Successful plant community restoration depends upon a close match between the desired plant species and the available pollination guilds. While some flowering plants have a generalized floral shape that can be pollinated by a large suite of pollinators, other plant species exhibit specialized zygomorphic shapes that restrict the range of potential pollinators (Handel 1997). The identity of the appropriate pollination guild can be determined by the examination of floral characters that are associated with different classes of pollinators (Barth 1985; Howe & Westley 1988). Provided that a given pollinator’s specific habitat needs can be met, reintroduction of native pollinators can be an inexpensive and effective method to restore pollination services (Nabhan 2001). To reintroduce native bee populations, bee nest trap boxes can be placed relatively undisturbed sites that contain the composition of vegetation that is most similar to the desired restoration goal. Specific bee genera can be attracted to the trap by varying the size of the entry holes. It is recommended that 25% of the pollinators in these traps should be re-released back into to the donor environment as not to significantly reduce the pollinator population (DOD technical report 2001).
Seed dispersers
Seed dispersers are an important consideration for plant restoration since they can enhance plant recruitment by reducing intraspecific plant competition, density dependent mortality, and seed predation. In addition, directed dispersal strategies can land seeds in favorable microsites and/or allow them to avoid unfavorable environmental conditions such as fire (Beattie 1985; Boyd 2001; Wenny 2001). Finally and probably most importantly dispersal can reduce the probability of local plant extinction and may act to accelerate successional processes (Whisenant 1999; McDonald 2000). The type of seed dispersers present can even dictate the distribution and composition of the plant community but unfortunately they may also be vectors of exotic seed (Handel 1997).
Establishing corridors between habitats
Like the pollinators, habitat linkage is also important for the survival and attraction of migratory and non-migratory seed dispersers (Dobson et al. 1999; Whisenant 1999). This connectivity between habitats can be achieved through a combination of several complementary restoration strategies. Again the current recommendations are the development of corridors that are least one home range in width (Dobson et al. 1999; Nabhan 2001) and the planting of many small clusters of pollinator specific vegetation to offer a continuous source of food, resting areas, and seeds (Whisenant 1999; McDonald 2000).
Attractant plants
Seed dispersers require an adequate food source and resting areas in order to successfully reoccupy an area. Often pollinator-specific “attractant” plant species are used to provide both a food source and resting area and sometimes to act as a route linking the restoration site to natural remnants (Handel 1997). For example, seed dispersing avian frugivores are often attracted to restoration sites by planting fleshy-fruited trees to serve as both a food source and a resting area. Likewise, Robinson & Handel (1993) hypothesized that the reason why many degraded lands remained weedy and fail to undergo natural succession is because avian seed dispersal was inhibited. They predicted that secondary succession could be initiated by attracting these “missing” avian seed dispersers. To test their hypothesis they planted 17 tree and shrub species in clusters across the degraded landfill site. They found that these clusters attracted avian seed dispersers, which in turn introduced 20 new species to the site after one year. Not only did the project reclaim a formerly economically and ecologically useless site, it also provided an important link between the surround natural forest remnants. Similarly, many restoration projects in Australia have utilized the planting of “perch trees” to attract avian and bat seed dispersers. In most cases, these cluster plants appear to be a viable and cost effective alternative to planting entire plant communities (McDonald 2000).
Artificial perches
Zanini & Ganade (2005) conducted a similar “perch tree” study in Brazil’s threatened subtropical Araucaria forest. However, instead of planting living trees for their experiment, they used artificial perches. They found that plant diversity and seed abundances were greater in the plots that contained perches than those that did not. In addition, artificial perches have been used in restoration projects as an attempt to mitigate the loss of vertical vegetative structure in Puerto Rican landslides. Shiels & Walker, (2003) found that these perches did increase the number of forest seeds on the exposed soil but this technique alone was not sufficient to completely stabilize the exposed soil. Therefore, artificial perches should probably be used in conjunction with other restoration methods in order to facilitate succession on a degraded site.
Future directions
Fungal endophytes form intercellular infections within plant tissues and exist asymptomatically for at least part of their life cycle (Saikkonen et al. 1998). These fungal symbionts can have significant effects on plant fitness (Clay 1998; Faeth 2004; Arnold et al 2003; Jumpponen & Trappe 1998) and the type of symbiosis can range from antagonistic and mutualistic (Faeth 2002). Although endophytes are a ubiquitous feature of nearly all plant species (Arnold et al. 2000; Schulthess & Faeth 1998), their ecological significance is often ignored. Perhaps this is because endophytes may have indirect effects on host fitness, community structure, and function that are not readily apparent under controlled single level laboratory analyses. Nevertheless these symbionts may eventually prove to be important components of future restoration projects.
Neotyphodium-grass interactions
Neotyphodium endophytes are obligate, asexual, seed-borne symbionts, which live intercelluarly within grass plant tissues. Evolutionary theory predicts that asexual symbionts should be strong mutualists because their reproductive success is tied to that of the host grass (Law 1985). Indeed, the Neotyphodium endophyte of some cool season grasses can interact mutualistically with its host plant and impart benefits such as drought tolerance, enhanced growth, pathogen resistance and herbivore deterrence however the strength and direction of this symbiotic interaction can vary with host species, environmental conditions, host genotypes, and fungal haplotypes (Faeth 2002; Hayes & Faeth 2002). In addition, the Neotyphodium endophyte have been shown to alter community structure, diversity and ecosystem processes such as productivity, community invasibility, and litter decomposition rates (Rudgers et al. 2005; Rudgers et al. 2004; Omacini et al. 2004). Therefore, land mangers should evaluate the effect of these endophytes on the individual level on many genetic and environmental backgrounds and at the community level on ecosystem processes prior to their incorporation into restoration efforts. Seed-borne endophyte viability is significantly reduced during long-term seed storage (Faeth 2002) and thus the success of restoration projects may be compromised if endophyte infection increases host persistence and survival, mediates competitive hierarchies between plant species, and/or alters the invasibility of the region.
Dark septate endophytes
The dark septate endophytes (DSEs) are a group of taxonomically unrelated fungi that commonly infection roots and the above ground tissue of a diverse range of plant species (Jumpponen & Trappe 1998). Some of these newly discovered symbionts appear to be mutualistic in that they improve plant survival under environmental stress. For example, Barrow & Aaltonen (2003) found that the hyphae of these fungi colonized the guard and subsidiary cells of their host, Bouteloua eripodia (Torr.) Torr. This evidence suggests that these endophytes may play a role in regulating stomatal function (and transpiration). Further, they found that the fungal hyphae formed a mucilagous matrix around the roots of this host, which could confer hydraulic connectivity and also act as a protective barrier to dry soil. In addition, the DSEs in four wing saltbush (Atriplex canescens (Pursh) Nutt.) have been shown to increase the solublization and uptake of phosphorus which in turn increased both shoot and root biomass of the host (Barrow & Avila-Osuna 2002). Finally, they assert that these endophyte act as plant carbon managers since they are closely associated with lipid bodies and these lipids are distributed throughout the roots (Barrow & Aaltonen 2001). Currently it is not known what factors might disrupt this symbiosis, however, I predict that these endophytic symbionts will become important restoration components in arid environments since they increase their host’s ability to survive drought and nutrient stress.
Conclusion
Clearly, plant mutualists are essential to the accurate restoration of ecosystem structure and function. Since some of these relationships are obligate for the plant partner, the restoration of self-perpetuating plant populations may not possible if corresponding mutualists are not considered. Conversely, vertically-transmitted (seed-borne) endophytes are obligate partners of plants and thus these “trapped pathogens” are predicted to evolve towards mutualism since their reproductive success is tied to that of the host plant. Perhaps then for restoration purposes, some plants should be considered as one component of a composite organism locked in tight association with its coevolved (or fortuitous) endophytes and as unit this plant/ fungus association may be dependent upon animal pollinators and seed dispersers for reproduction, dissemination and survival. Undoubtedly, this multi-trophic view of ecological restoration will continue to yield success stories in the future, however, a great deal of basic research is still necessary to detail the secret lives of most native pollinators, seed dispersers and endophytic fungi.
Additional Resources
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