Differential effectiveness of novel and old legume–rhizobia mutualisms: implications for invasion by exotic legumes

Abstract

The degree of specialization in the legume-rhizobium mutualism and the variation in the response to different potential symbionts are crucial factors for understanding the process of invasion by exotic legumes and the consequences for the native resident plants and bacteria. The enhanced novel mutualism hypothesis predicts that exotic invasive legumes would take advantage of native rhizobia present in the invaded soils. However, recent studies have shown that exotic legumes might become invasive by using exotic introduced microsymbionts, and that they could be a source of exotic bacteria for native legumes. To unravel the role of novel and old symbioses in the progress of invasion, nodulation and symbiotic effectiveness were analyzed for exotic invasive plants and native co-occurring legumes in a Mediterranean coastal dune ecosystem. Although most of the studied species nodulated with bacteria from distant origins these novel mutualisms were less effective in terms of nodulation, nitrogenase activity and plant growth than the interactions of plants and bacteria from the same origin. The relative effect of exotic bradyrhizobia was strongly positive for exotic invasive legumes and detrimental for native shrubs. We conclude that (1) the studied invasive legumes do not rely on novel mutualisms but rather need the co-introduction of compatible symbionts, and (2) since exotic rhizobia colonize native legumes in invaded areas, the lack of effectiveness of these novel symbiosis demonstrated here suggests that invasion can disrupt native belowground mutualisms and reduce native legumes fitness.

Mutualistic Interactions and Biological Invasions

“…Most show high levels of nodulation in invaded ranges, indicating either that effective rhizobia are widely distributed between continents and/or that many legumes can nodulate with a wide range of rhizobia strains (Rodríguez-Echeverría et al 2011, Ndlovu et al 2013. For some invasive legumes, however, novel mutualisms appear to be less effective in terms of nodulation, nitrogenase activity, and plant growth than the interactions of plants and bacteria of the same origin (Rodríguez-Echeverría et al 2012). Other studies have shown that alien legumes may become invasive by using alien microsymbionts (Rodríguez-Echeverría 2010).…”

Invasive Lespedeza cuneata and native Lespedeza virginica experience asymmetrical benefits from rhizobial symbionts

“…Previous studies have implicated Bradyrhizobium strains in supporting exotic legume invasions in New Zealand (Weir et al 2004), Australia (Lafay and Burdon 2006), Africa (Boukhatem et al 2012;Ndlovu et al 2013 Boukhatem et al 2012). Finally, there are a number of reports of co-invasion by exotic legumes and their associated Bradyrhizobium bacteria (Lafay and Burdon 2006;Leary et al 2006;Rodriguez-Echeverria 2010;Rodriguez-Echeverria et al 2012). In conjunction with the widespread reports of Bradyrhizobium associations with plant invasions, the large asymmetry Bradyrhizobium-associated plant growth for invasive and native Lespedeza reported here makes Bradyrhizobium a likely candidate genus for further study in regards to L. cuneata invasion.…”

“…It would be very interesting to know if the disproportionate benefits of L. cuneata reported here extend to these other kinds of symbioses. Different strains of microbial symbionts can have differential fitness effects on different plant hosts (Cardinale et al 2008;Helgason et al 2002;Rangin et al 2008;Rincon-Rosales et al 2009;RodriguezEcheverria et al 2012;van der Heijden et al 1998), and these differential effects may be related to the degree of "familiarity" between the host and the symbiont (Klironomos 2003;Rodriguez-Echeverria 2010;Rodriguez-Echeverria et al 2012). For example, in a Mediterranean dune system, the legume-rhizobium symbiosis leads to higher nodulation rates, nitrogenase activity, and plant growth when native legumes are paired with native rhizobacteria and when exotic legumes are paired with rhizobacteria from their home range (Rodriguez-Echeverria et al 2012;Thrall et al 2007).…”

“…Consequently, some invasive legumes do not appear to be limited by the density or community composition of soil rhizobia (Birnbaum et al 2012). However, the legume-rhizobium symbiosis is more effective when invasive Acacia are matched with bacteria from their home range in comparison with native bacteria (Rodriguez-Echeverria et al 2012;Thrall et al 2007). The legume Leucaena leucocephala failed to survive in its invaded range until its corresponding symbiotic rhizobia were introduced (Richardson et al 2000).…”

Research on mutualisms between native and non-native partners can contribute critical ecological insights

“…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 1), and such work may build on the strong foundation in novel mutualism research established by scientists working to understand the importance of positive interactions in a context of biological invasions (e.g., Richardson et al 2000;Klironomos 2003;Ness 2003;Traveset and Richardson 2006;Aizen et al 2008;Kaiser-Bunbury et al 2011;Rodríguez-Echeverría et. al.…”