Secondary invasion: When invasion success is contingent on other invaders altering the properties of recipient ecosystems

Abstract

Positive interactions between exotic species may increase ecosystem‐level impacts and potentially facilitate the entry and spread of other exotic species. Invader‐facilitated invasion success—”secondary invasion”—is a key conceptual aspect of the well‐known invasional meltdown hypothesis, but remains poorly defined and empirically underexplored. Drawing from heuristic models and published empirical studies, we explore this form of “secondary invasion” and discuss the phenomenon within the recognized conceptual framework of the determinants of invasion success. The term “secondary invasion” has been used haphazardly in the literature to refer to multiple invasion phenomena, most of which have other more accepted titles. Our usage of the term secondary invasion is akin to “invader‐facilitated invasion,” which we define as the phenomenon in which the invasion success of one exotic species is contingent on the presence, influence, and impacts of one or more other exotic species. We present case studies of secondary invasion whereby primary invaders facilitate the entry or establishment of exotic species into communities where they were previously excluded from becoming invasive. Our synthesis, discussion, and conceptual framework of this type of secondary invasion provides a useful reference to better explain how invasive species can alter key properties of recipient ecosystems that can ultimately determine the invasion success of other species. This study increases our appreciation for complex interactions following invasion and highlights the impacts of invasive species themselves as possible determinants of invasion success. We anticipate that highlighting “secondary invasion” in this way will enable studies reporting similar phenomena to be identified and linked through consistent terminology.

Secondary invasion re‐redefined: The distinction between invader‐facilitated and invader‐contingent invasions as subclasses of secondary invasion

“…In their recent article in Ecology and Evolution , O'Loughlin and Green (2017) set out to (1) redefine the term secondary invasion as the condition “when invader success is contingent on other invaders altering the properties of recipient ecosystems” and (2) propose a framework for accounting for this phenomenon in invasion ecology. We applaud the second objective.…”

“…The authors provide many examples of invader‐facilitated invasions in describing their framework, but their review generated only two cases that may actually meet the stringent criteria of secondary invaders being obligatorily facilitated by a primary invader (i.e., Grosholz et al., 2000; O'Dowd, Green, & Lake, 2003). While many invaders may facilitate secondary invasions and invaders that are strong mutualists and ecosystem engineers may in some cases open doors to secondary invaders that were otherwise so tightly closed as to preclude entry (e.g., Grosholz et al., 2000; O'Dowd et al., 2003), the bulk of the cases of invader‐facilitated invasions are arguably examples of primary invaders (or even concurrent or later invaders) facilitating other invaders that were not excluded from the system (e.g., Flory & Bauer, 2014; see also examples in Kuebbing & Nuñez, 2015; O'Loughlin & Green, 2017; Simberloff, 2006; Simberloff & Von Holle, 1999; White, Wilson, & Clarke, 2006). A general finding from invasion ecology is that most communities are open to invasion (Callaway & Maron, 2006), and there are surprisingly few examples of invaders that are physiologically capable of establishing in a system but are otherwise completely excluded (Mack, 1996).…”

Surrogacy in invasion research and management: inferring “impact” from “invasiveness”

“…However, it is well established that impact is also a function of per capita effects, which in turn are mediated by environmental factors independent of the invader; as such, invasiveness should not be expected to be a consistent surrogate for impact across time and space (Dick et al . ; O'Loughlin and Green ; Sofaer et al . ).…”

“…). For instance, the invasive giant African land snail ( Achatina fulica ) establishes and spreads within the rainforests on Christmas Island only after that ecosystem has been altered by other invasive taxa (O'Loughlin and Green ), and high densities of the snail do not have the measurable impacts on seedling recruitment or leaf litter dynamics that would be expected based on the snail's known traits and behaviors observed elsewhere (Figure b; O'Loughlin and Green ). Therefore, any measure of this species’ presence, abundance, functional traits, or impacts in a different setting would misrepresent the ecological impacts of this invasion.…”

“…Demonstrating and predicting the impacts of invasive species on recipient ecosystems is difficult due to the highly context‐specific interactions and drivers that characterize most invasions (Courchamp et al . ; O'Loughlin and Green ). Closing this knowledge gap represents an ongoing challenge for invasion research and management.…”