Biological invasions can threaten ecosystems ¹ , economies ² , and human health ³ . The Scientific Committee on Problems of the Environment (SCOPE) put biological invasions on top of its research agenda in 1983 ⁴ . Since then, the field of invasion ecology has rapidly gained momentum. The number of publications dealing with biological invasions has increased a hundredfold in less than two decades ⁵ . Several journals are partly (e.g. Diversity and Distributions, Natural Areas Journal) or fully (e.g. Biological Invasions, Invasive Plant Science and Management, NeoBiota) devoted to research, management and policy issues related to invasive species. However, despite a growing body of knowledge on biological invasions, difficulties remain in predicting invasion success ⁶ .

Within Europe, the distribution of people is strongly related to the number of alien species. Presumably, this reflects that biological invasions are aided by human transport and that species establishment is facilitated by human disturbance ⁷ . Nevertheless, at the global scale, the proportion of widely distributed alien plant species (relative to all species) is far lower in Europe than in North America – despite Europe’s long history of trade and therefore a longer residence time of alien plants ⁸ . The observation that Europe serves as a global contributor of alien plant species, whereas North America seems to be a better recipient, has sparked the concept of biological resistance, which explains invasion success or failure in relation to the traits of the native flora ⁹ . An additional important consideration, which has not been assessed to date, could be that Europe also has a higher proportion of landscapes that are actively managed by humans than, for example, the Americas, Australia and Africa ¹⁰ . To date, approaches to predict invasion patterns in response to anthropogenic global change have focused on (i) the extent of novel ecosystems ¹¹ , and (ii) alien species richness ¹² .

In this paper, we propose that the abundance of an alien species in a given landscape can be (at least partly) explained by the level of active landscape maintenance by humans. We term this hypothesis the Human Release Hypothesis. As discussed in detail below, the Human Release Hypothesis states that the abundance of invasive species may be partly explained by the level of human activity or landscape maintenance, with intermediate levels of human activity providing optimal conditions for high abundance. Unlike the Disturbance Hypothesis and the Intermediate Disturbance Hypothesis, which explain patterns of establishment of invasive species ¹³ and patterns of native species diversity respectively ¹⁴ , the Human Release Hypothesis specifically addresses patterns in the abundance of alien species that are already established in particular areas outside their native ranges.

We first discuss how the Human Release Hypothesis fits into the context of other key hypotheses in invasion ecology. We then illustrate the hypothesis via a case study on a global invader, the sweetbriar rose ( Rosa rubiginosa L.). Finally, we assess how the Human Release Hypothesis may be integrated into biological invasion research, and we hypothesize which locations worldwide may be particularly prone to supporting high abundances of invasive species.

According to Richardson et al. (2000) ¹⁵ , an invasive terrestrial plant species is a naturalized alien species that produces reproductive offspring, often in very large numbers, at considerable distance from parent plants, and thus has the potential to spread over extensive areas. A key question in invasion ecology is how the interaction of species traits with environmental characteristics predicts invasion success, including both establishment and abundance in the new environment ⁶ .

Catford et al. (2009) ¹⁶ summarized 29 leading hypotheses predicting invasion success and integrated them into the PAB-framework ( Figure 1). This framework considers the size and frequency of introductions (i.e. propagule pressure, P), ecosystem invasibility based on abiotic characteristics of the new environment (A), and biotic characteristics of an invasive species and its recipient community (B). In this framework, human influence on the invasion process is recognized primarily during the establishment stage. For example, human action can increase propagule pressure ¹⁷ and multiple introduction events make establishment more likely, because species have a higher chance to encounter suitable environmental conditions ¹⁸ . Multiple introductions of the same species also can lead to higher genetic diversity ¹⁹ . However, examples exist of successful invaders with low genetic diversity ²⁰ , and stemming from single or few introduction events, suggesting that propagule pressure is only one of many variables explaining invasion patterns ²¹ .

With respect to abiotic conditions, invasion is facilitated if species are pre-adapted to their new environment, for example due to a similar climate in the new environment ²² . Like propagule pressure, pre-adaption is not a necessary precondition for successful invasion, because climatic niche shifts have been reported for invasive species ²³ . Disturbance events also provide windows of opportunity for invasive species ²⁴ . Many invasive plant species are adapted to exploit temporarily favourable conditions through their short life cycles, rapid growth, high reproductive allocation, persistent soil seed banks and rapid germination (the Ideal Weed Hypothesis) ²⁵ .

Finally, biotic characteristics of the recipient community may involve the absence of natural enemies. The Enemy Release Hypothesis explains invasion success as a function of alien species having escaped their natural enemies, allowing them to allocate resources to growth and reproduction rather than defence ²⁶ . This would make alien plants stronger competitors. In the context of the Intermediate Disturbance Hypothesis, which proposes higher species diversity at intermediate frequencies or intensities of disturbance (see Wilkinson, 1999) ¹⁴ , alien plants are likely to have the greatest impact on community diversity when resources become limited and plant diversity is highest, by co-opting more resources ²⁷ .

In parallel to the Enemy Release Hypothesis, here, we propose the Human Release Hypothesis. It describes a situation where alien species have escaped relatively higher levels of human landscape maintenance that is characteristic within their native ranges. Changing patterns of land use are widely recognized to increase opportunities for introduced species to establish and spread ²⁸ , but already prevailing patterns of land use intensity also should be expected to influence the populations of species – both in their native and introduced ranges. This is because highly intensive land use by humans (such as in many parts of Western Europe) often corresponds to high levels of active landscape maintenance – which translates into little available habitat for both native and introduced species, as well as high levels of active weed control. At the other end of the spectrum of human land use intensity, we hypothesize that pristine natural habitats also offer few windows of opportunity for alien species to establish (the Biotic Resistance Hypothesis) ²⁹ . Thus, we hypothesize that the abundance of invasive species should be highest in between these two extremes – namely in extensively used landscapes characterized by frequent fallowing, low levels of weed control, high heterogeneity, and many disturbed edges of small farmland patches ³⁰ . Such landscapes are where “human release” should contribute to optimal conditions for invasive species to establish large populations.

While existing hypotheses explain the establishment and naturalization process of invasions, little work has attempted to explain the (potential) abundance of invasive species in their new environments. Part of this gap may be effectively addressed by the Human Release Hypothesis ( Figure 1).

To illustrate the plausibility of the Human Release Hypothesis, we present findings at two scales on the invasion success of Rosa rubiginosa, a shrub native to Eurasia and invasive in Australia, New Zealand, South Africa, North and South America (see Dataset 1 and Supplementary Figure S1). First, we synthesize previous cross-continental case studies that compared plant performance between invasive populations in Central and Southern Argentina with native populations in Spain and Germany (for more details see Zimmermann et al., 2012) ³¹ . Second, we compare climatic conditions as well as land use and human population density between invasive and native R. rubiginosa populations at a global scale. In combination, our findings suggest the Human Release Hypothesis may be a useful complementary hypothesis to other existing hypotheses in invasion biology ( Table 1).

Rosa rubiginosa has successfully invaded a range of ecosystems within Argentina, covering a major climatic gradient, but exhibiting low levels of genetic diversity ^{32, 33} ( Figure 2a). Low genetic diversity suggests that multiple introduction events constituting particularly high propagule pressure cannot explain the species' invasion success. Despite lower genetic diversity, populations of R. rubiginosa are considerably smaller in Spain and Germany than in Argentina ( Figure 3) – native populations consist of 5 to 20 individuals whereas invasive populations consist of hundreds of individuals ³¹ . In addition to propagule pressure, abiotic and biotic variables also cannot fully explain the invasion success of R. rubiginosa. In Argentina, the species neither benefits from favourable soil conditions nor from reduced biotic resistance ³¹ .

Moreover, a global climatic analysis shows that R. rubiginosa also does not depend or benefit from pre-adaptation to the climate of its new environment ( Figure 2b). We developed two climatic envelope models based on BioClim parameters and the occurrence of native and invasive populations respectively using the maximum entropy method ³⁴ (MAXENT, see Appendix 1 and 2 in the Supplementary material). We detected a significant differentiation of realized niches between invasive and native populations (Schoener’s D=0.31, p<0.0001; Figure 2b). Furthermore, back-projection of the climatic niche based on invasive populations points to a southern European origin. However, genetic analyses tracked the native origin of invasive Argentinean, Chilean, Australian and New Zealand populations to Central Europe ^{32, 33} . Key climatic predictors therefore do not point to a climatic advantage in the invasive range, but instead indicate that R. rubiginosa is able to thrive under a wide range of conditions ( Supplementary Figure S2 and Supplementary Figure S3).

The Ideal Weed and Disturbance Hypotheses ( Table 1) partly explain the invasion success of R. rubiginosa in Argentina ^{31, 35, 36} . However, the Enemy Release Hypothesis failed to explain abundance patterns – natural enemies appeared equally harmful to the species in the native and introduced ranges ³¹ ( Table 1). By contrast, in the invasive range, anthropogenic disturbances such as logging and burning create windows of opportunities for the rose to establish, but just as importantly, disturbance events are then followed by decades of abandonment that enable the species to become abundant.

Having considered a wide range of existing hypotheses ( Table 1), we found that additional insights into the invasion patterns of R. rubiginosa may be gained by the Human Release Hypothesis. This is because a key difference between native and introduced environments appears to be the level of active landscape maintenance. In the case study, we observed frequent trimming or removal of individuals only in Spain and Germany and not in Argentina, and individuals and populations in Argentina were significantly older than their native counterparts ^{31, 36} . At the global scale, our analysis revealed a similar pattern (albeit at a coarser resolution; 2.5 × 2.5 arc min, Figure 2c). Native R. rubiginosa populations occur in areas with higher proportions of cropland, residential areas and human population densities than invasive populations ( Figure 2c). These conditions very likely correspond to a high degree of landscape maintenance, and hence little available habitat for R. rubiginosa in its native range.

A key premise of this paper is that existing hypotheses that predict invasion success can be effectively complemented by the Human Release Hypothesis ( Figure 1). Our own data, of course, focused only on one species – which is enough to pose a hypothesis, but far too little to test its general usefulness. To that end, we see two research priorities that should be addressed to further scrutinize the Human Release Hypothesis so that, if appropriate, it can be integrated into invasive species management. First, additional species should be studied in both their native ranges and in different parts of their introduced ranges. Such comparisons would be useful to test the drivers of invasive species abundance and to validate (or refute) invasion patterns derived from modelling approaches ^{11, 12} . An important first clue that the Human Release Hypothesis may be relevant could be whether invasive individuals of a given perennial species are significantly older than individuals within the native range. Second, it may be useful to further investigate the relationship between landscape maintenance and human land use intensity, how it manifests in different regions, and if generalizations are possible at the global scale. The frequency of weeding and trimming, as well as the prevalence of fallowing, are just two of many potential indicators for the level of active landscape maintenance.

Evidently, the Human Release Hypothesis is still in its infancy, and it would be unwise to make bold management recommendations on its basis. Based on our analysis to date, preliminary insights that are relevant to managing invasive species are: (i) sparsely populated areas may face a higher risk of biological invasions than more densely populated areas; (ii) extensively managed rangelands may be more susceptible to high abundances of invasive species than intensively managed croplands; and (iii) high abundances of invasive species at landscape and regional scales could be facilitated by long periods of fallowing or land abandonment ³⁷ .

The data referenced by this article are under copyright with the following copyright statement: Copyright: � 2014 Zimmermann H et al.

Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

figshare: Dataset 1. Rosa rubiginosa L. occurrence data (occurrences_R.rubiginosa.csv, 416 kb). Doi: 10.6084/m9.figshare.1002067 ³⁸