Plant–soil interactions limit lifetime fitness outside a native plant’s geographic range margin

Abstract

Plant species’ distributions are often thought to overwhelmingly reflect their climatic niches. However, climate represents only a fraction of the n‐dimensional environment to which plant populations adapt, and studies are increasingly uncovering strong effects of nonclimatic factors on species’ distributions. We used a manipulative, factorial field experiment to quantify the effects of soil environment and precipitation (the putatively overriding climatic factor) on plant lifetime fitness outside the geographic range boundary of a native California annual plant. We grew plants outside the range edge in large mesocosms filled with soil from either within or outside the range, and plants were subjected to either a low (ambient) or high (supplemental) spring precipitation treatment. Soil environment had large effects on plant lifetime fitness that were similar in magnitude to the effects of precipitation. Moreover, mean fitness of plants grown with within‐range soil in the low precipitation treatment approximated that of plants grown with beyond‐range soil in the high precipitation treatment. The positive effects of within‐range soil persisted in the second, wetter year of the experiment, though the magnitude of the soil effect was smaller than in the first, drier year. These results are the first we know of to quantify the effects of edaphic variation on plant lifetime fitness outside a geographic range limit and highlight the need to include factors other than climate in models of species’ distributions.

Host‐specific soil microbes contribute to habitat restriction of closely related oaks (Quercusspp.)

“…Our finding implies that species habitat distributions are more than a simple function of abiotic constraints. Particularly, we demonstrate that considering the effects of soil microbial communities and the phylogenetic relationships among host plants will be essential to fully capture the factors determining fine‐scaled plant distributions (Benning & Moeller, 2020 , 2021 ; Kempel et al, 2018 ; McCarthy‐Neumann & Ibáñez, 2012 ; Pither et al, 2018 ). We encourage future studies and native plant conservation to account for the effects of belowground biotic interactions on species habitat preferences and habitat partitioning.…”

“…For instance, when the annual plant Clarkia xantiana ssp. xantiana was transplanted beyond its habitat, soil microbes decreased lifetime fitness of the transplanted individuals while the home‐range live soil improved the fitness (Benning & Moeller, 2020 ). Other transplant experiments also found survival of the transplanted species to be restricted by the presence of soil fungal pathogens or the absence of soil mutualists (Brown & Vellend, 2014 ; Carteron et al, 2020 ).…”

“…On the other hand, biotic interactions can also limit geographic distributions of a host species. Particularly, the roles of seed predators, herbivores, and soil microbes on species distributions is an active area of research (Alexandre et al, 2018 ; Benning & Moeller, 2020 ; Gaston, 2009 ; McCarthy‐Neumann & Ibáñez, 2012 ). However, most of these studies have not linked these biotic interactions among close relatives with habitat restriction, that is, limited occurrence of a species to certain habitat(s) within its geographic range.…”

Rules of Plant Species Ranges: Applications for Conservation Strategies

“…Mutualisms are abundant in stressful conditions (Callaway et al, 2002), affect plant fitness (Lau and Lennon, 2012), mitigate climate stress on species distributions (Bulleri et al, 2016), and influence local adaptation (Pickles et al, 2015). Facultative mutualisms can facilitate expansion of species ranges into stressful habitats (Afkhami et al, 2014;Millar and Bennett, 2016;Benning and Moeller, 2021b) in addition to novel environments (Crotty and Bertness, 2015;Bueno de Mesquita et al, 2020). A key example of a mutualism that expands the plant realized niche is pollination (Phillips et al, 2020).…”

Legume germination is delayed in dry soils and in sterile soils devoid of microbial mutualists: Species‐specific implications for upward range expansions

“…Additionally, agricultural studies have demonstrated that some soil microbial species are able to promote host seed germination by excreting phytohormones, thereby increasing germination success in newly colonized habitats (Atzorn et al, 1988 ; Noel et al, 1996 ; Bastian et al, 1998 ; Tsavkelova et al, 2007 ; Miransari & Smith, 2009 ; Kumar et al, 2011 ; Namvar & Sharifi, 2011 ; Meena et al, 2012 ; Ngumbi & Kloepper, 2016 ; Wu et al, 2016 ). Conversely, the absence of mutualists can negatively affect population persistence and limit species distributions (Benning & Moeller, 2021b ; Harrower & Gilbert, 2018 ; Mueller et al, 2011 ; Nuñez et al, 2009 ; Pellmyr, 2003 ). Indeed, this has been documented in some soil microbe–plant mutualisms (Simonsen et al, 2017 ; Stanton‐Geddes & Anderson, 2011 ).…”