Ecological facilitation

Facilitation describes species interactions that benefit at least one of the participants and cause harm to neither (Stachowicz 2001). Facilitations can be categorized as mutualisms, in which both species benefit, or commensalisms, in which one species benefits and the other is unaffected. Much of classic ecological theory ("e.g.", natural selection, niche separation, metapopulation dynamics) has focused on negative interactions such as predation and competition, but positive interactions (facilitation) are receiving increasing focus in ecological research (Boucher "et al." 1982, Callaway 1995, Stachowicz 2001, Bruno "et al." 2003, Tirado and Pugnaire 2005). This article addresses both the mechanisms of facilitation and the increasing information available concerning the impacts of facilitation on community ecology.

Categories

There are two basic categories of facilitative interactions.:# A "mutualism" is an interaction between species that is beneficial to both. A familiar example of a mutualism is the relationship between flowering plants and their pollinators (Boucher "et al." 1982, Callaway 1995). The plant benefits reproductively from the spread of pollen between flowers, while the pollinator receives some form of nourishment, either from nectar or the pollen itself. :# A "commensalism" is an interaction in which one species benefits and the other species is unaffected. Epiphytes (plants growing on other plants, usually trees) have a commensal relationship with their host plant because the epiphyte benefits in some way ("e.g.", by escaping competition with terrestrial plants or by gaining greater access to sunlight) while the host plant is apparently unaffected (Callaway 1995).

Strict categorization, however, is not possible for some complex species interactions. For example, seed germination and seedling survival in harsh environments is often higher under so-called nurse plants than on open ground (Callaway 1995, Stachowicz 2001). A nurse plant is one with an established canopy, beneath which conditions for seed germination and seedling survival are less harsh due to increased shade, soil moisture, and nutrients. Thus, the relationship between seedlings and their nurse plants is commensal. However, as the seedlings grow into established plants, they are likely to compete with their former benefactors for resources (Callaway 1995, Stachowicz 2001).

Mechanisms

The beneficial effects of species on one another are realized in various ways, including refuge from physical stress, predation, and competition, improved resource availability, and transport.

Refuge from physical stress

Facilitation may act by reducing the negative impacts of a stressful environment (Callaway 1995, Stachowicz 2001, Bruno "et al." 2003, Tirado and Pugnaire 2005). As described above, nurse plants facilitate seed germination and seedling survival by alleviating stressful environmental conditions. A similar interaction occurs between the red alga "Chondrus crispus" and the canopy-forming seaweed "Fucus" in intertidal sites of southern New England, USA (Stachowicz 2001). The alga survives higher in the intertidal zone—where temperature and desiccation stresses are greater—only when the seaweed is present because the canopy of the seaweed offers protection from those stresses. The previous examples describe facilitation of individuals or of single species, but there are also instances of a single facilitator species mediating some community-wide stress, such as disturbance. An example of such “whole-community” facilitation is substrate stabilization of cobble beach plant communities in Rhode Island, USA, by smooth cordgrass ("Spartina alterniflora": Bruno 2000). Large beds of cordgrass buffer wave action, thus allowing the establishment and persistence of a community of less disturbance-tolerant annual and perennial plants below the high-water mark.

In general, facilitation is more likely to occur in physically stressful environments than in physically favorable environments, where competition may be the most important interaction among species (Callaway 1995, Stachowicz 2001, Bruno "et al." 2003, Tirado and Pugnaire 2005). This can also occur in a single habitat containing a gradient from low to high stress. For example, along a New England, USA, salt marsh tidal gradient, Bertness and Hacker (1994) found that presence of black needle rush ("Juncus gerardi") increased the fitness of marsh elder ("Iva") shrubs in lower elevations, where soil salinity was higher. The rush shaded the soil, which decreased evapotranspiration, and in turn decreased soil salinity. However, at higher elevations where soil salinity was lower, marsh elder fitness was decreased in the presence of the rush, due to increased competition for resources. Thus, the nature of species interactions may shift with environmental conditions.

Refuge from predation

Another mechanism of facilitation is a reduced risk of being eaten. Nurse plants, for example, not only reduce abiotic stress, but may also physically impede herbivory of seedlings growing under them (Callaway 1995). In both terrestrial and marine environments, herbivory of palatable species is reduced when they occur with unpalatable species (Callaway 1995, Stachowicz 2001, Bruno "et al." 2003). These “associational refuges” may occur when unpalatable species physically shield the palatable species, or when herbivores are “confused” by the inhibitory cues of the unpalatable species (Callaway 1995, Stachowicz 2001). Herbivory can also reduce predation of the herbivore, as in the case of the red-ridged clinging crab ("Mithrax forceps") along the North Carolina, USA, coastline (Miller and Hay 1996). This crab species takes refuge in the branches of the compact ivory bush coral ("Oculina arbuscula") and feeds on seaweed in the vicinity of the coral. The reduced competition with seaweed enhances coral growth, which in turn provides more refuge for the crab. A similar case is that of the interaction between swollen-thorn acacia trees ("Acacia" spp.) and certain ants ("Pseudomyrmex" spp.) in Central America (Boucher "et al." 1982). The acacia provides nourishment and protection (inside hollow thorns) to the ant in return for defense against herbivores. In contrast, a different type of facilitation between ants and sap-feeding insects may increase plant predation (Boucher "et al." 1982). By consuming sap, plant pests such as aphids produce a sugar-rich waste product called honeydew, which is consumed by ants in exchange for protection of the sap-feeders against predation.

Refuge from competition

Another potential benefit of facilitation is insulation from competitive interactions. Like the now familiar example of nurse plants in harsh environments, “nurse logs” in a forest are sites of increased seed germination and seedling survival because the raised substrate of a log frees seedlings from competition with plants and mosses on the forest floor (Harmon and Franklin 1989). The crab-coral interaction described above is also an example of refuge from competition, since the herbivory of crabs on seaweed reduces competition between coral and seaweed (Miller and Hay 1996). Similarly, herbivory by sea urchins ("Strongylocentrotus droebachiensis") on kelps ("Laminaria" spp.) can protect mussels ("Modiolus modiolus") from overgrowth by kelps competing for space in the subtidal zone of the Gulf of Maine, USA (Witman 1987).

Improved resource availability

Facilitation can increase access to limiting resources such as light, water, and nutrients for interacting species. For example, epiphytic plants often receive more direct sunlight in the canopies of their host plants than they would on the ground (Callaway 1995). Also, nurse plants increase the amount of water available to seedlings in dry habitats because of reduced evapotranspiration beneath the shade of nurse plant canopies (Callaway 1995). However, the most familiar examples of increased access to resources through facilitation are the mutualistic transfers of nutrients between symbiotic organisms. A symbiosis is a prolonged, close association between organisms, and some examples of mutualistic symbioses include::# Gut flora—associations between a host species and a microbe living in the host’s digestive tract, wherein the host provides habitat and nourishment to the microbe in exchange for digestive services. For example, termites receive nourishment from cellulose digested by microbes inhabiting their gut (Boucher "et al." 1982).:# Lichens—associations between fungi and algae, wherein the fungus receives nutrients from the alga, and the alga is protected from harsh conditions causing desiccation (Boucher "et al." 1982).:# Corals—associations between reef-building corals and photosynthetic algae called zooxanthellae, wherein the zooxanthellae provide nutrition to the corals in the form of photosynthate, in exchange for nitrogen in coral waste products (Stachowicz 2001).:# Mycorrhizae—associations between fungi and plant roots, wherein the fungus facilitates nutrient uptake (particularly nitrogen) by the plant in exchange for carbon in the form of sugars from the plant root (Boucher "et al." 1982). There is a parallel example in marine environments of sponges on the roots of mangroves, with a relationship analogous to that of mycorrhizae and terrestrial plants (Stachowicz 2001).

Transport

The movement by animals of items involved in plant reproduction is usually a mutualistic association. Pollinators may increase plant reproductive success by reducing pollen waste, increasing dispersal of pollen, and increasing the probability of sexual reproduction at low population density (Boucher "et al." 1982). In return, the pollinator receives nourishment in the form of nectar or pollen (Boucher "et al." 1982). Animals may also disperse the seed or fruit of plants, either by eating it (in which case they receive the benefit of nourishment) or by passive transport, such as seeds sticking to fur or feathers (Boucher "et al." 1982, Bruno "et al." 2003).

Community Effects

Although facilitation is often studied at the level of individual species interactions, the effects of facilitation are often observable at the scale of the community, including impacts to spatial structure, diversity, and invasibility.

patial structure

Many facilitative interactions directly affect the distribution of species. As discussed above, transport of plant propagules by animal dispersers can increase colonization rates of more distant sites, which may impact the distribution and population dynamics of the plant species (Boucher "et al." 1982, Bruno "et al." 2003, Tirado and Pugnaire 2005). Facilitation most often affects distribution by simply making it possible for a species to occur in a site where some environmental stress would otherwise prohibit growth of that species. This is apparent in whole-community facilitation by a foundation species, such as sediment stabilization in cobble beach plant communities by smooth cordgrass (Bruno 2000). A facilitating species may also help drive the progression from one ecosystem type to another, as mesquite apparently does in the grasslands of the Rio Grande Plains, USA (Archer 1989). As a nitrogen-fixing tree, mesquite establishes more readily than other species on nutrient-poor soils, and following establishment, mesquite acts as a nurse plant for seedlings of other species (Callaway 1995). Thus, mesquite facilitates the dynamic spatial shift from grassland to savanna to woodland across the habitat (Archer 1989).

Diversity

Facilitation affects community diversity (defined in this context as the number of species in the community) by altering competitive interactions. For example, intertidal mussels increase total community species diversity by displacing competitive large sessile species such as seaweed and barnacles (Bruno "et al." 2003). Although the mussels decrease diversity of primary space holders (i.e., large sessile species), a larger number of invertebrate species are associated with mussel beds than with other primary space holders, so total species diversity is higher when mussels are present (Bruno "et al." 2003). The effect of facilitation on diversity could also be reversed, if the facilitation creates a competitive dominance that excludes more species than it permits (Stachowicz 2001).

Invasibility

Facilitation of non-native species, either by native species or other non-native species, may increase the invasibility of a community, or the ease with which non-native species become established in a community. In an examination of 254 published studies of introduced species (non-native species brought to a community by humans, whether purposefully or accidentally), Simberloff and Van Holle (1999) found that 22 of 190 interactions studied between introduced species in the studies were facilitative. It is worth noting that 128 of the 190 examined interactions were predator-prey relationships of a single plant-eating insect reported in a single study, which may have overemphasized the importance of negative interactions. Introduced plants are also facilitated by native pollinators, dispersers, and mycorrhizae (Richardson 2000). Thus, positive interactions must be considered in any attempt to understand the invasibility of a community.

Conclusion

Facilitation is clearly a significant ecological process that produces community-level effects through interactions between individuals. By improving dispersal, increasing access to resources, and providing protection from stress, predation, and competition, facilitation can impact community structure, diversity, and invasibility. Incorporation of facilitation into such classic theories as natural selection and niche separation should be a goal of current and future ecologists. This will require further research into the mechanisms of facilitation at the level of individuals, and the impacts of facilitation at the level of population, community, and ecosystem. Continued study of positive species interactions will serve to improve our understanding of ecological processes and application of ecological theories.

References

*Archer, S. 1989. Have southern Texas savannas been converted to woodlands in recent history? American Naturalist 134: 545-561.
*Bertness, M. D. and S. D. Hacker. 1994. Physical stress and positive associations among marsh plants. American Naturalist 144: 363-372.
*Boucher, D. H., S. James, and K. H. Keeler. 1982. The ecology of mutualism. Annual Review of Ecology and Systematics 13: 315-347.
*Bruno, J. F. 2000. Facilitation of cobble beach plant communities through habitat modification by Spartina alterniflora. Ecology 81:1179-1192.
*Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory. TREE 18: 119-125.
*Callaway, R. M. 1995. Positive interactions among plants (Interpreting botanical progress). The Botanical Review 61: 306-349.
*Harmon, M. E. and J. F. Franklin. 1989. Tree seedlings on logs in Picea-Tsuga forests of Oregon and Washington. Ecology 70: 48-59.
*Miller, M. W. and M. E. Hay. 1996. Coral-seaweed-grazer-nutrient interactions on temperate reefs. Ecological Monographs 66: 323-344.
*Richardson, D. M. "et al." 2000. Plant invasions—the role of mutualisms. Biological Review 75: 65-93.
*Shears N.T.; Babcock R.C. (2007) Quantitative description of mainland New Zealand's shallow subtidal reef communities. "Science for Conservation 280". p 126. Published by Department of Conservation, New Zealand [http://www.doc.govt.nz/upload/documents/science-and-technical/sfc280entire.pdf]
*Simberloff, D. and B. Van Holle. 1999. Positive interactions of non-indigenous species: invasional meltdown? Biological Invasions 1: 21-32.
*Stachowicz, J. J. 2001. Mutualism, facilitation, and the structure of ecological communities. BioScience 51: 235-246.
*Tirado, R. and F. I. Pugnaire. 2005. Community structure and positive interactions in constraining environments. OIKOS 111: 437-444.
*Witman, J. D. 1987. Subtidal coexistence: storms, grazing, mutualism, and the zonation of kelps and mussels. Ecological Monographs 57: 167-187.