The Human Release Hypothesis for biological invasions: human activity as a determinant of the abundance of invasive plant species

Introduction

Biological invasions can threaten ecosystems¹, economies², and human health³. The Scientific Committee on Problems of the Environment (SCOPE) put biological invasions on top of its research agenda in 1983⁴. 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 decades⁵. 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 success⁶.

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 disturbance⁷. 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 plants⁸. 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 flora⁹. 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 Africa¹⁰. To date, approaches to predict invasion patterns in response to anthropogenic global change have focused on (i) the extent of novel ecosystems¹¹, and (ii) alien species richness¹².

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 species¹³ and patterns of native species diversity respectively¹⁴, 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.

The Human Release Hypothesis

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 environment⁶.

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 pressure¹⁷ and multiple introduction events make establishment more likely, because species have a higher chance to encounter suitable environmental conditions¹⁸. Multiple introductions of the same species also can lead to higher genetic diversity¹⁹. However, examples exist of successful invaders with low genetic diversity²⁰, and stemming from single or few introduction events, suggesting that propagule pressure is only one of many variables explaining invasion patterns²¹.

Figure 1. Incorporating our hypothesis into the PAB framework.

The establishment and abundance of invasive plant species are explained by different mechanisms, which have been summarized by Catford et al. (2009)¹⁶ in the PAB framework (see text for details). However, the biological characteristics of a given invading species and of its new environment only partly explain the abundance of established invasive populations. We argue that additional insights can be gained via the Human Release Hypotheses, which can complement the existing PAB framework.

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 environment²². Like propagule pressure, pre-adaption is not a necessary precondition for successful invasion, because climatic niche shifts have been reported for invasive species²³. Disturbance events also provide windows of opportunity for invasive species²⁴. 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 defence²⁶. 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 resources²⁷.

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 spread²⁸, 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 patches³⁰. 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).

Case study on an invasive rose

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 individuals³¹. 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 resistance³¹.

Figure 2. Rosa rubiginosa benefits from human release.

(a) Genetic diversity in Rosa rubiginosa is higher in its native Spanish and German populations than in the introduced populations in Argentina, suggesting the species did not benefit from multiple introductions (for details see Zimmermann et al. 2010)³². (b) The species does not benefit from a climatic pre-adaptation to the new range. The world map shows the species' climatic niche based on the species’ native distribution (blue) and the invasive distribution (pink). Overlap of climatic niches (purple) is minimal. (c) Rosa rubiginosa appears to benefit from “human release” in its new range. The barplot shows the global proportions of different anthropogenic biomes¹⁰ according to the location of invasive and native sweetbriar rose populations. The native range has a larger proportion of residential areas and a higher human population density (log people/km²). Only 0.56% of the invasive range is wildlands, and only 0.03% of the native range.

Figure 3. Invasive Rosa rubiginosa populations in Argentina (a, b) and native populations in Germany (c) and Spain (d).

In parts of Argentina, single disturbance events have offered windows of opportunity for the species to establish populations, some of which have remained undisturbed for 30 years or longer (a)^31,36. The low level of human landscape maintenance means that populations can expand over vast areas and consist of hundreds of individuals (a, here along the whole visible lakeside in Patagonia). (a) For our study area in Patagonia we predicted that 36% of the area (5000 km²) was threatened by R. rubiginosa invasion, across a precipitation gradient from 1400 mm/annum (mountains in the far background) to 600 mm/a³⁶. In Argentina R. rubiginosa shrubs have time to grow to their full size (b), by contrast, many native landscapes are regularly maintained; shrubs are regularly trimmed and mostly grow in hedgerows (c, Germany). Furthermore, in Germany and Spain, fewer habitats are available in landscapes dominated by agriculture and urban areas (d, Spain).

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 method³⁴ (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 ranges³¹ (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.

Integrating the Human Release Hypothesis with other explanations

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 abandonment³⁷.

Data availability

figshare: Dataset 1. Rosa rubiginosa L. occurrence data (occurrences_R.rubiginosa.csv, 416 kb). Doi: 10.6084/m9.figshare.1002067³⁸