Commentary |
Corresponding author: Clare E. Aslan ( clare.aslan@nau.edu ) Academic editor: Mark van Kleunen
© 2015 Clare E. Aslan, Benjamin A. Sikes, Keryn B. Gedan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Aslan CE, Sikes BA, Gedan KB (2015) Research on mutualisms between native and non-native partners can contribute critical ecological insights. NeoBiota 26: 39-54. doi: 10.3897/neobiota.26.8837
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Mutualisms are important structuring forces in ecological communities, influencing ecosystem functions, diversity, and evolutionary trajectories. New interactions, particularly between native and non-native species, are globally increasing in biotic communities as species introductions accelerate. Positive interactions such as novel mutualisms can affect the fitness of organisms in invaded communities. Non-natives can augment native mutualism networks, replace extinct native partners, or disrupt native mutualisms. Because they are actively forming or newly formed, novel mutualisms offer a unique opportunity to examine in real time the factors governing early mutualism formation and stability, including frequency-dependent processes and those relying on specific traits or functions. These central ecological questions have been inferred from long-formed mutualisms, but novel mutualisms may allow a glimpse of successes and failures in ecological time with insights into the relative importance of these factors as ecological systems shift. To this end, this commentary addresses how novel mutualisms inform our understanding of mutualism formation, stability, the importance of functional traits, and niche vs. neutral processes, using examples across multiple systems. Novel mutualism research thus far has been largely limited in both questions and ecosystems, but if more broadly applied could benefit both theoretical and applied ecology.
Positive interactions, marine, belowground, biological invasions, non-native species, novel mutualisms
Mutualisms are thought to be ubiquitous across habitat types (
Ecologically and evolutionarily, mutualisms have shaped many biological invasions and vice versa (recently reviewed by
Because it focuses on early mutualism stages (rather than inferences from later stages), novel mutualism research may improve our understanding of the foundation for mutualisms more generally as well as the implications of potential mutualist introductions. This commentary uses specific examples of novel mutualisms to discuss early mutualism formation and stability, the role of functional traits, and niche vs. neutral processes in community assembly. Novel mutualism research to date has been heavily concentrated in the realms of invasion biology and aboveground, terrestrial ecosystems. We deliberately discuss traits of novel mutualisms across ecological domains to seek broad patterns relevant to these new avenues of research.
Scientific literature uses a variety of definitions for the term “mutualism.” The simplest, conventional definition for mutualism is any interaction between two species that results in fitness benefits for both species (notated as “+/+”) (
Glossary of terms describing interspecific interactions.
Mutualism: an interaction wherein both sides derive fitness benefits and the interaction occurs at the individual level (“+/+”). |
Facilitation: an interaction wherein at least one species derives a fitness benefit and the other side is not detrimentally affected. |
Obligate: an interaction necessary for survival of one or both of the species involved. (Antonym: Facultative) |
Specific: an interaction in which a species has only a single partner or very small number of partners. (Antonym: General) |
Diffuse: an interaction involving many species or a network. (Antonym: Pairwise) |
Basic evolutionary and ecological research focused on emergent ecosystem properties has explored the factors driving mutualism formation. Benefits of mutualisms can be contextual (
Conceptual figure of the formation and stability of novel mutualisms by niche and neutral processes at different stages of invasion. The x-axis represents three general stages of a biological invasion as necessary for mechanistic purposes, despite substantial debate in the literature about how invasion stages should be delineated. The y-axis represents the formation of novel mutualisms and the dotted line represents the shifting relative abundance of the non-native species. Red areas represent limitation of novel mutualism formation by the process described; green areas represent enhancement or reinforcement by the process described. Hashed vertical lines represent filters: the mutualism formation filter may be imposed by functional traits in the non-native organism or by niche traits preventing mutualism formation. Once the mutualism has formed and the species has spread, mutualism specialization filters may be imposed by strong selection for certain mutualistic traits; increased specialization may impact mutualism stability.
Thus, novel mutualisms appear to recapitulate a general mutualism tendency to be facultative, particularly early in the mutualism formation process. Known facultative novel mutualisms include most novel seed dispersal relationships (e.g.,
To our knowledge, there are only two documented examples of novel mutualisms in marine systems. One such novel marine mutualism is also facultative. The native sediment dwelling polychaete Diopatra cuprea in the mid-Atlantic U.S. incorporates the invasive red alga Gracilaria vermiculophylla into its decorated tube caps (
Does the lack of other marine examples of novel mutualisms arise from a dearth of research or from a true lack of novel mutualism formation? The few other relevant research attempts in marine systems have failed to detect novel mutualisms. For example, an unusual zooxanthella found in a native Hawaiian coral, once considered a novel mutualism, is instead of cryptogenic origin (
Research on novel mutualisms may also help us understand why some early mutualisms fail while others result in long-term associations. A focus of mutualism stability research is partner fidelity in the presence of “cheaters” (
Since generality logically confers increased stability and reduces dependence on cheating or at-risk partners, it is unsurprising that mutualism network literature has demonstrated that generality is extremely common (e.g.,
Classic research on mutualism formation and stability also quantifies traits of mutualistic partners as potential limiting reagents that have led to the mutualisms present today. Functional traits form the foundation of many mutualistic networks. For example, pollination syndromes and functional groups of effective partners can generally be defined by flower morphology, color, and reward type of a plant species (
How then, do newly arriving non-native species fit into an existing landscape of functional traits and functional group partnerships within a community? Trait-based methods can distinguish environmental filtering and community-level niche partitioning (
In contrast to interspecific competition, a strong effect of mutualism on community assembly would select for non-native species with traits that link easily into existing mutualism networks, effectively favoring species that have traits more similar to native mutualists (Fig.
As incipient partnerships, novel mutualisms also offer a unique opportunity to assess the relative importance of interaction frequency as driven by abundance, a neutral process, with that of adaptive traits that provide specific mutualistic benefits defined by the niches of their potential partners (
The importance of niche and neutral processes in novel mutualisms could change during the invasion process as a non-native species initially establishes at low density, spreads and often increases in abundance, and ultimately is integrated into the community. As outlined above, non-native species requiring specific mutualisms are unlikely to establish because they may not find suitable partners. This limitation is largely niche-based. After establishment, non-native species that become problematically invasive may be present at much higher abundance than native partners. While an abundant non-native can reduce the stability of native mutualisms (
The relative importance of neutral vs. niche processes may also be explored through mutualistic network models. For example, asymmetric specialization or nestedness is a pervasive feature of known mutualistic networks (
As our discussion illustrates, novel mutualisms may serve as prototypes for the study of mutualism formation and thresholds in mutualism strength and exploitation. Using novel mutualisms as model systems to better understand how species enter and establish in communities may help advance basic research and fill current understanding gaps. Because they are widespread and dynamic, novel mutualisms are promising focal points for a diversity of outstanding basic questions (Table
Examples of questions in ecology and evolutionary biology that could be addressed with novel mutualisms as focal systems.
Research questions |
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Basic ecology |
Do novel mutualisms promote stability, resilience, and diversity in ecological communities, as native-native mutualisms appear to do? |
Do mutualistic networks containing non-native species demonstrate the same architectural traits or level of stability as native networks? |
Do novel mutualisms result from availability of open ecological niches? |
Might specialization, at the level of the non-native or native interactors, dictate whether novel mutualisms can form? |
When non-natives establish in interaction networks, to what degree and in what ways are they redundant with native participants? |
Are some types of interaction networks more easily invaded? |
Are invaded networks more or less resilient to future extinctions than non-invaded networks? |
Evolutionary biology |
What can the formation of novel mutualisms—where coevolutionary history is lacking—tell us about mutualism evolution? |
Do non-native mutualists impose or respond to the same selective pressures as native mutualists, and what are the evolutionary implications of novel mutualisms for native species? |
A diversity of modern research challenges may benefit from a better understanding of mutualism formation and stability and of the roles of functional traits and niche and neutral processes in emergent ecosystem properties. As one example, we can focus on microbial mutualisms, increasingly being recognized as critical players in a wide diversity of previously-unknown contexts (
Biological invasions will continue to foment novel mutualisms in every system, with unforeseen consequences for native communities. These organisms provide unprecedented opportunity to observe the early stages of interaction development, and to directly observe processes that can be addressed only inferentially using traditional study systems and species. We suggest that novel mutualisms represent an excellent test arena for current understanding of mutualism formation, mutualism stability, functional traits, and niche vs. neutral processes. Novel mutualisms lend themselves to an expanded set of questions and research systems. Expansion and deepening of novel mutualism research can create synergy between invasion biology, basic ecology, and evolutionary biology, to the mutual benefit of all three.
The development of this manuscript benefitted greatly from discussions with many of the SCB Smith Fellows, from logistical support from S. Foster and M. Dombeck, and from conversations with J. DeBose, J. Stachowicz, and E. Sotka. We thank M. Rejmánek and N. Blüthgen for several helpful comments on early drafts, and several anonymous reviewers for encouraging us to seek novel approaches with this manuscript. The research was supported by David H. Smith Conservation Research Fellowships to CA, BS, and KG.