Viewing Emerging Human Infectious Epidemics through the Lens of Invasion Biology

1 Viewing emerging human infectious epidemics through the lens of invasion biology 1 2 Montserrat Vilà1,2*, Alison M. Dunn3, Franz Essl4, Elena Gómez-Díaz5, Philip E. Hulme6, Jonathan M. 3 Jeschke7, Martín A. Núñez8,9, Richard S. Ostfeld10, Aníbal Pauchard11,12, Anthony Ricciardi13, Belinda 4 Gallardo14,15 5 1Estación Biológica de Doñana (EBD-CSIC), Avd. Américo Vespucio 26, 41092 Isla de la Cartuja, 6 41092 Sevilla, Spain (montse.[email protected]) ORCID: 0000-0003-3171-8261 7 2Department of Plant Biology and Ecology, University of Sevilla, C/Profesor García González S/N, 8 41012 Sevilla, Spain 9 3Faculty of Biological Sciences, University of Leeds, LS2 9JT UK ([email protected]) ORCID: 0000-10 0002-4855-1077 11 4Bioinvasions. Global Change. Macroecology Group, Department of Botany and Biodiversity 12 Research, University Vienna, Rennweg 14, 1030 Vienna, Austria (franz.ess[email protected]) ORCID: 13 0000-0001-8253-2112 14 5Institute of Parasitology and Biomedicine Lopez-Neyra (IPBLN-CSIC), Avda. del Conocimiento, 15 17, 18016 Armilla, Granada, Spain ([email protected]) ORCID: 0000-0002-4146-9003 16 6Bio-Protection Research Centre, Lincoln University, PO Box 85084, Canterbury, New Zealand 17 ([email protected]) ORCID: 0000-0001-5712-0474 18 7Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 310, 12587 19 Berlin, Germany; Institute of Biology, Freie Universität Berlin, Königin-Luise-Str. 1-3, 14195 Berlin, 20 Germany; Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Königin-Luise-21 Str. 2-4, 14195 Berlin, Germany ([email protected]) ORCID 0000-0003-3328-4217 22 8Grupo de Ecología de Invasiones, INIBIOMA, CONICET, Universidad Nacional del Comahue, 23 Pioneros 2350, San Carlos de Bariloche 8400, Argentina ([email protected]) ORCID: 0000-0003-24 0324-5479 25 9Department of Biology and Biochemistry, University of Houston, Houston, Texas, 77204 USA 26 10Cary Institute of Ecosystem Studies, Millbrook, New York 12545, USA 27 ([email protected]) ORCID: 0000-0002-3707-9301 ORCID: 0000-0003-1284-3163 28 11Laboratorio de Invasiones Biológicas (LIB). Facultad de Ciencias Forestales, Universidad de 29 Concepción, Victoria 631, Concepción, Chile; ([email protected]) 30 12Institute of Ecology and Biodiversity (IEB), Santiago, Chile. 31 13Redpath Museum, McGill University, Montreal, Quebec, H3A 0C4 Canada 32 ([email protected]) ORCID: 0000-0003-1492-0054 33 2 14Pyrenean Institute of Ecology (IPE-CSIC), Avda. Montañana 1005, 50059 Zaragoza, Spain 34 (beli[email protected]) ORCID: 0000-0002-1552-8233 35 15BioRISC (Biosecurity Research Initiative at St Catharine’s), St Catharine’s College, Cambridge, CB2 36 1RL, UK 37 *Corresponding author 38 39 MV designed and led the manuscript. All coauthors contributed to the investigation, interpretation 40 and writing of the manuscript. BG designed all the figures. 41 42 3 Abstract 43 Invasion biology examines species originated elsewhere and moved with the help of humans, and 44 their impacts on biodiversity, ecosystem services, and human well-being. In a globalized world, the 45 emergence and spread of many human infectious pathogens are quintessential biological invasion 46 events. Some macroscopic invasive species themselves contribute to the emergence and 47 transmission of human infectious agents. We review conceptual parallels and differences between 48 human epidemics and biological invasions by animals and plants. Fundamental concepts in 49 invasion biology regarding the interplay of propagule pressure, species traits, biotic interactions, 50 eco-evolutionary experience, and ecosystem disturbances can help to explain transitions between 51 stages of epidemic spread. As a result, many forecasting and management tools used to address 52 epidemics could be applied to biological invasions and vice versa. Thus, we advocate for increasing 53 cross-fertilization between both disciplines to improve prediction, prevention, treatment, and 54 mitigation of invasive species and infectious disease outbreaks, including pandemics. 55 56 Keywords: biosecurity, immunology, introduced species, One Health, SARS-CoV-2 57 58 4 Introduction 59 Invasive species – i.e. non-native (alien, exotic) species that have been introduced to new regions 60 by humans , form self-sustaining populations and spread rapidly from the sites of introduction 61 (Blackburn et al. 2011, Essl et al. 2018) – can have enormous impacts on the environment, the 62 economy and human well-being (Vilà and Hulme 2016, Pyšek et al. 2020). Invasion biology, a 63 discipline examining the ecological, evolutionary and anthropogenic processes involved in the 64 spread and impact of non-native species, has mostly focused on free-living, conspicuous 65 macroscopic species, which spread is observable and easy to track. In contrast, the invasion 66 dynamics of parasites and pathogens have received less attention, except for those causing 67 damage to agriculture, forestry and livestock (but see Mallon et al. 2015, Thakur et al. 2019, Pyšek 68 et al. 2020). More recently, the focus has expanded to include pathogens that affect wildlife 69 (Hatcher et al. 2012, Dunn and Hatcher 2015, Roy et al. 2017). The emergence and spread of 70 human infectious agents that rapidly increase in incidence and geographic area can also be viewed 71 as a biological invasion, but have rarely been treated as such (Hatcher et al. 2012, Nuñez et al. 72 2020) – although many studies have described the direct and indirect human health impacts of 73 biological invasions, including those involving the introduction of human pathogens (Hatcher et al. 74 2012, Rabitsch et al. 2017). 75 A human pathogen can spread beyond its historical range and become invasive, usually as a result 76 of the movement of infected human hosts. In addition to humans assisting the spread of invasive 77 animal and plant species, invasive species themselves can facilitate the large-scale propagation of 78 human pathogens and epidemics by acting as vectors or reservoir hosts of emerging human 79 pathogens, or by providing habitat for them (Fig. 1). Indeed, 16 % of the IUCN list of 100 of the 80 World’s Worst Invasive Alien Species (Lowe et al. 2000) promote the spread and impact of human 81 pathogens (Table 1). Invasive insects are the most frequent vectors of pathogens causing human 82 diseases (Lounibos 2002). For example, the tiger mosquito (Aedes albopictus) has spread to all 83 inhabited continents through trade and is a vector of several infectious pathogens including those 84 causing dengue fever, yellow fever, West Nile Virus (WNV) and Chikungunya (Gratz 2004, Enserink 85 2008). Another group of invasive mosquitoes are some Anopheles spp., the most important 86 vectors of Plasmodium spp., the blood parasites that cause malaria (Lounibos 2002, Takken and 87 Lindsay 2019). Invasive vertebrates such as rodents are frequent reservoirs or intermediate hosts 88 of human pathogens (Hatcher et al. 2012, Hulme 2014a). Finally, invasive species, particularly 89 plants, can create habitat conditions conducive to local proliferation of vector or reservoir hosts 90 (Mack and Smith 2011, Rai and Singh 2020). For example, the invasive bush Lantana camara 91 attracts and provides refuge for tsetse flies away from river courses and close to villages, 92 promoting sleeping sickness epidemics (Syed and Guerin 2004). Similarly, water hyacinth, 93 Eichhornia crassipes, forms dense mats that provide breeding habitat for mosquitoes that transmit 94 Plasmodium (causative agent of malaria), Filofilaria immitis (filariasis) or Flaviviruses (dengue 95 fever) (Mack and Smith 2011). These cases exemplify the enormous diversity of combinations of 96 native-invasive pathogen, host and reservoir that are possible (Fig. 2), suggesting myriad potential 97 roles of invasive species in the ecology and global spread of pathogens (Rabitsch et al. 2017). 98 Both biological invasions and infectious diseases are becoming more prevalent and widespread 99 with globalization. Both phenomena share common drivers of introduction and spread (Mack et al. 100 2000, Jeschke et al. 2013). In biological invasions, there has been a substantial amount of research 101 on species traits conferring invasion potential (i.e. invasiveness), on the vulnerability of the 102 ecosystems to be invaded (i.e. invasibility), and on the role of environmental conditions facilitating 103 or preventing spread (Pyšek et al. 2012). Similarly, research on infectious diseases mainly focuses 104 5 on understanding factors influencing the ability to establish persistent infections and cause 105 disease (i.e. virulence) and on the transmission from host to host (i.e. transmission), why some 106 microorganisms and specific strains cause disease, which individuals and human populations are 107 more susceptible to infection, and how/which environmental conditions affect pathogen spread 108 (Horrocks et al. 2011). However, because research on invasions and epidemics are approached by 109 different disciplines, the bodies of literature and terminology are usually separated (Box 1). An 110 exchange and cross-fertilization between both research domains is needed to advance the 111 prevention, treatment and adaptation of their impacts (Conn 2009, Ogden et al. 2019, Hulme et al. 112 2020, Nuñez et al. 2020). 113 The introductions of invasive species and human pathogens have been described as co-occurring 114 phenomena caused by the transport of species, including people, during early European 115 colonization of the Americas, and some African and Asian territories during the XV-XVII centuries 116 (Crosby 2004, Spinage 2012). There are historical descriptions, for instance, of how these human 117 migration patterns led to disease outbreaks in the new territories (e.g. influenza, smallpox, and 118 measles). However, despite epidemiology having acknowledged the ecological aspects of 119 infectious diseases since its start, and invasion biology having some of its foundations in the 120 spread and impacts of pathogens – e.g. Elton (1958) highlighted several examples of plant, animal 121 and human pathogens as biological invasions, the formal interaction between both disciplines is 122 quite recent and currently limited: the number of publications bridging the two disciplines is 123 several orders of magnitude lower than in each field separately (Fig. 3). 124 Approaches such as One Health, EcoHealth, Planetary Health and One Biosecurity emphasizes the 125 links between human health, environmental health, and the health of plants and animals (Ogden 126 et al. 2019, Hulme 2021). Following this principle, there have been recent attempts to cross-127 fertilize research on biological invasions and human infectious diseases both from conceptual and 128 methodological perspectives. While marked differences do exist in the ecology and evolution of 129 human pathogens and free-living macroscopic invasive species, including issues of host specificity, 130 immunity as well as the temporal and spatial scales of interactions, opportunities exist to bring 131 these disciplines together under a common framework (Lewis et al. 2016, Hulme et al. 2020). 132 Previous reviews have mostly focused on the stages of invasions and emerging infectious 133 pathogens, especially those that also affect wildlife (Hatcher et al. 2012, Jeschke et al. 2013, Dunn 134 and Hatcher 2015, Roy et al. 2017); on the role of invasive species as vectors and/or reservoirs of 135 pathogens worldwide (Hulme 2014a, Rabitsch et al. 2017); or on spatial dynamics (Hulme et al. 136 2020). Most of these interdisciplinary approaches have been on particular taxa, habitats or regions 137 (Crowl et al. 2008, Medlock et al. 2012, Conn). Yet, a detailed review of the parallels between 138 scientific approaches to invasions and human epidemics is still missing. 139 140 Given increasing rates of emerging infectious pathogens and biological invasions worldwide, and 141 the on-going global health crisis caused by the novel coronavirus SARS-CoV-2, the need for 142 integrative and interdisciplinary approaches to biosecurity has never been greater (Nuñez et al. 143 2020, Pyšek et al. 2020, Hulme 2021). Here, we provide a holistic review of key parallels in the 144 conceptual foundations in invasion biology and human infectious epidemics. Specifically, we (1) 145 describe approaches to the study of the pathways of introduction of invasive species and human 146 pathogens; (2) compare the stages and dynamics of the invasion process with those of epidemics; 147 (3) outline well-established hypotheses on the performance and impacts of invasive species, and 148 show their analogues in human pathogens; (4) summarize the usefulness and limitations of 149 forecasting tools; and finally (5) discuss the implications for biosecurity. 150 6 Pathways of introduction of invasive species and transmission of pathogens 151 With globalization, the numbers of invasive species and human pathogens has increased 152 exponentially in the 20th century, with no sign of saturation (Jones et al. 2008, Seebens et al. 153 2017). Invasive species including pathogens are rapidly transported by the same global networks 154 that move products and people to distant regions, where they are likely to encounter naïve 155 ecological and human communities that have not interacted with them before. For example, 156 dengue virus, the causative agent of dengue fever, is expanding its distribution range and it is now 157 reported in 128 countries. The main factor of its spread is related to climatic change that benefits 158 the Aedes aegypti mosquito, the main vector of the virus, and increased human movements 159 between populations; even sporadic indigenous virus transmissions have occurred in previously 160 dengue-free countries (Chomicz et al. 2016). Managing the pathways of introduction of invasive 161 species and infectious pathogens is a prerequisite to implementing effective surveillance, early 162 response and mitigation policies (Essl et al. 2015, Ogden et al. 2019). 163 The Convention on Biological Diversity (CBD) provides a global standard terminology for species 164 introduction pathways that can be classified by six mechanisms: release, escape, transported as 165 contaminant, transported as stowaway, corridors and unaided (Saul et al. 2017). These can be 166 further classified in 44 subcategories that identify their socioeconomic use and purpose of 167 introduction (e.g. horticulture, pet trade, fisheries, game, etc.). Recently, this classification has 168 been applied to thousands of non-native species introduced to Europe and worldwide (Pergl et al. 169 2020). Range-expansion of native species that track environmental changes is an ecological 170 phenomenon that gets often confounded with biological invasions. However, there are major 171 functional, phylogenetic, physiological, behavioural and phenology feature differences separating 172 range-expanding from non-native species (Essl et al. 2019); accordingly, both groups of species 173 deserve to be treated as distinct biogeographic entities (Essl et al. 2020). Range-expanding species 174 (i.e. neonatives) can also cause environmental and health impacts (Wallingford et al. 2020). 175 However, to not increase the complexity of our review, we do not include range-expanding species 176 in this study. 177 In human epidemiology, besides the dichotomy between active and passive introduction of 178 pathogens (Mallon et al. 2015), a classification of pathways to such detail as in biological invasions 179 is currently not available. The term ‘pathways of introduction’ refers to the movement of the 180 pathogen either as a free-living stages (environmental contamination), or via the original 181 (reservoir) host, the vector or by human hosts. Infected hosts that travel with their newly acquired 182 pathogens to distant places contribute to their geographical spread. Phylogenetic and genomic 183 analyses are important tools used to reconstruct epidemiological origin, history and links among 184 infectious hosts. Genomic surveillance is not routinely used in biological invasions to identify the 185 geographic origin and pathways of introduction of non-native macroorganisms (but see Hamelin 186 and Roe 2020). 187 Transmission of emerging infectious pathogens can also be classified as zoonotic or non-zoonotic. 188 A global analysis suggests that more than 60 % of human emerging infectious pathogens are 189 zoonotic, with 70 % of these originating in wildlife (Jones et al. 2008). The IUCN list 100 of the 190 World’s Worst Invasive Alien Species contains twelve species that are reservoirs of pathogens that 191 infect humans (Table 1). The most well-known historical example is the house mouse (Mus 192 musculus) and the black rat (Rattus rattus) as hosts of Yersinia pestis causing bubonic plague. 193 Other invasive species include the small Indian mongoose, Herpestes javaricus, and the crab eating 194 macaque (Macaca fascicularis) as reservoirs for rabies. Zoonoses, by definition, involve pathogen 195 7 spillover from a vertebrate host to humans, although subsequent human-to-human transmission 196 is sometimes possible. These host-switching events from wildlife reservoir to human can be 197 preceded by an invasion event, e.g., when the reservoir host enters a previously unoccupied area 198 (e.g., wildlife transported to an urban market), or followed by an invasion event, e.g. when 199 infected people travel, with their newly acquired pathogens, to distant places. Zoonotic spillover is 200 seen for multiple pathogens including Plasmodium spp. (causative agent of malaria), Trypanosoma 201 brucei (trypanosomiasis) , Leishmania sp. (leishmaniasis), influenza A (flu), Human Immune 202 Deficiency Virus (AIDS), Ebolavirus (Ebola haemorrhagic disease) as well as the new coronavirus 203 related to MERS-CoV and SARS-CoV (Karesh et al. 2012). 204 In invasion biology, prevention requires an analysis of how the invasive species likely will arrive to 205 a new region (primary introduction) and how it spreads subsequently in the surrounding region 206 (secondary spread). This dual pathway classification has seldom been applied in emerging 207 infectious pathogens despite that it is well known that socioeconomic variables (e.g. behavior, 208 income, tourism, military deployment, trade, etc.) can highly influence transmission. An improved 209 understanding of mechanisms that link longand short-distance pathogen spread with the 210 socioeconomic characteristics of the hosts is essential to prevent and manage epidemics. 211 Stages and dynamics of invasions and epidemics 212 There are several distinct terms used to describe processes of invasion and those of an epidemic; 213 but conceptually, the invasion of ecosystems and the infection process at the individual and 214 population level follow essentially the same basic series of stages, i.e. transport/exposure, 215 introduction/infection, establishment/transmission and spread/epidemics, respectively (Jeschke et 216 al. 2013, Dunn and Hatcher 2015, Plowright et al. 2017, Hulme et al. 2020, Nuñez et al. 2020). In 217 both cases, whether a particular invasive species or pathogen is able to pass on to the next stage 218 and has consequences for the receiving ecosystem or host depends on many filters and can be 219 substantially influenced by human interventions (Fig. 4). These stages have used different 220 terminology for invasions and infections, respectively, as indicated below. 221 Transport/exposure. International transport of the non-native species by human agency is the first 222 stage of the biological invasion process. Similarly, in emerging infectious pathogens, international 223 movement of hosts (e.g. planes or boats) represents the first contact (or exposure) of humans 224 with infected human hosts. The pathogen may originate in wildlife or domestic vertebrates and 225 spillover to humans either through a vector (e.g. insects) or through direct contact (i.e zoonosis). 226 Introduction/Infection. Following transport, some non-native species are released directly into the 227 wild (e.g. for fishing or hunting purposes) escape from captivity (e.g. pets) or cultivation (e.g. 228 ornamental plants), or move unaided utilizing artificial corridors (e.g. waterways). A pathogen can 229 also be introduced through released and escaped reservoirs or move unaided through air (e.g. air-230 conditioning) or water (e.g. sewage) infrastructures. For a pathogen, at the individual host level, 231 this is the infection stage where it enters the host body, circumventing behavioral, physical and 232 physiological barriers. Many human infectious pathogens such as Hendra virus, WNV or the strain 233 of Influenza A causing avian flu result from independent spillover from reservoirs with little 234 human-to-human transmission. These outbreaks tend to be short-lived, but nonetheless can have 235 high impact in humans (e.g. the case fatality rate for some avian flu is 60%, Greger 2007). 236 Establishment/Transmission. Establishment of an invasive species is the process by which a 237 founding non-native population reproduces, increases in size and becomes self-sustaining in the 238 new range. Invasive species introduced to a new region have to overcome several biotic and 239 8 environmental barriers imposed by the recipient region and its biota (Blackburn et al. 2011). For a 240 pathogen, at the level of the individual host, this is equivalent to overcoming immunological 241 barriers that allow within-host persistence, its multiplication and transmission to new hosts. 242 Widespread transmission and establishment within a new host population occurs when the basic 243 rate of reproduction (R0, the number of secondary cases resulting from each primary case) 244 exceeds 1. The likelihood of the pathogen evolving to become self-sustaining in the human 245 population increases with the spillover rate, the current R0 and the mutation rate (Antia et al. 246 2003). For example, during the 2013-2016 Ebola virus outbreak, three adaptive mutations in the 247 virus genome occurred that affected the functional activity of various viral proteins increasing its 248 ability to enter human cells, grow and be transmitted (Urbanowicz et al. 2016). 249 Spread. Finally, spread is the process by which an invasive species expands its range in the 250 introduced region beyond the area or host population in which it was first established. This 251 matches with the definition of epidemics as the spread of the pathogen to many persons in a 252 locality during a short period. Such an expansion of a pathogen in a human population can occur 253 through increased animal-to-human contacts (spillover) or through human-to-human 254 transmission. For human infectious pathogens, spread can occur anywhere along a gradient from 255 transmission between individuals in a local population, to global transport of infections between 256 populations. Like biological invasions in general, the large scale spread of pathogens follows hub-257 and-spoke network dynamics, and does not occur homogeneously but rather in discrete, 258 sometimes lengthy jumps, facilitated by human transportation systems such as air travel 259 (Strickland et al. 2015). The most serious outcome of an emerging pathogen is a pandemic – an 260 epidemic occurring worldwide, or over a very wide area, crossing international boundaries and 261 usually affecting a large number of people. 262 Unprecedented opportunities for pathogen spread and transmission are generated by (1) 263 technological advances and social activities driving human mobility, as evident in the movement of 264 millions of humans between continents on a daily basis (Tatem et al. 2006), and (2) with 265 increasingly crowded living conditions and inadequate access to water, sanitation, and health care, 266 in many areas of the world. For example, the first cases of Sars-CoV2 in many countries were 267 associated to business and tourism, whereas subsequent local spread was mainly related to 268 factors such as housing density and occupational exposure (Bassino and Ladmiral 2020). Owing to 269 global transportation networks, introduced organisms – both pathogens and free-living 270 macroscopic species – create satellite outbreaks in distant regions that contribute to exponential 271 rates of spatial expansion. 272 Rate of spread. There are temporal and spatial differences in the dynamics of epidemics and 273 invasions. In an epidemic, the speed by which the pathogen can spread is usually faster than the 274 invasion of a free-living macroscopic species (Peterson 2008). The spread of human epidemic 275 pathogens can be explosive. It is generally one to three orders of magnitude faster than for 276 invasive species and plant pathogens (Fig. 5). This is due to their short generation times, high 277 mutational rate and by orders of magnitude higher effective population sizes. Rates of spread of 278 terrestrial flora and fauna are typically in the range of 0.1-100 km/yr (Hulme 2014b, Horvitz et al. 279 2017) with mobile species such as many invertebrates (e.g. forest pest insects) being faster 280 (Roques et al. 2016). In contrast, human epidemic viruses such as Zika, Ebola and West Nile Virus, 281 can spread at rates of 103–104 km/year (Zinszer et al. 2015, 2017, Hadfield et al. 2019), a velocity 282 only reached in some pathogens of marine wildlife (McCallum et al. 2003). 283 9 These differences in spread velocity matter because they influence the response of the recipient 284 systems in many ways. For instance, rapid range expansion could render phenotypic or genotypic 285 adjustments in recipient populations and communities less likely. Moreover, success in the control 286 of invasive species and infectious pathogen spread is highly dependent on the spatial distribution 287 of introductions (Hulme et al. 2020). Scattered nascent foci of invasive species or infested hosts 288 have the potential to spread more rapidly than one large continuous focus (Moody and Mack 289 1988). The recommendation to detect, isolate and trace every contact of the SARS-CoV-2 infected 290 individual follows this principle (e.g. Pagliari 2020). 291 Lag times. This phenomenon has received a fair amount of attention in invasion biology to define 292 the duration between invasion stages, and also between the introduction and the onset of rapid 293 range expansion (Crooks 2005, Rouget et al. 2016, Spear et al. 2021). Lag times are particularly 294 evident in ornamental plant species that only start to spread after several decades of being 295 introduced (Kowarik 1995). Many populations of non-native plants are dependent on repeated 296 introductions and need a long residence time before they form self-sustaining, viable populations 297 (Dlugosch and Parker 2008). Small populations are very sensitive to environmental stochasticity 298 that might limit their survival, reproduction and dispersal during early stages of invasion (Mack 299 2000). There are many cases of non-native species that were unnoticed for a long time and only 300 became invasive as a response to environmental changes. 301 Lag times are also identified in emerging human pathogens, owing to the latency period between 302 infection and disease symptoms that can range from a few days (e.g. SARS-CoV) to years (e.g. HIV). 303 More precise time intervals than for invasions are defined for pathogens in terms of stages of the 304 pathogen life-cycle and disease symptoms (Bar-On et al. 2020). For example, in virus infections, 305 time lags within an individual host are decomposed into (1) the eclipse period as the time to make 306 intracellular virions; (2) the latent period as the time from cell entry until the appearance of the 307 first extracellular viruses; (3) the infectious period (from infection to transmission) and (4) the 308 incubation period (from infection to the emergence of symptoms). The length of these four 309 periods are of paramount importance to slow down and deter the transmission stage to an 310 epidemic spread by establishing quarantine and confinement periods. 311 Many invasive species that are vectors of human parasites are increasing their ranges induced by 312 global warming (Medlock and Leach 2015). Similarly, many infectious diseases are increasing with 313 climate change e.g. by speeding up the life cycle of the pathogens. For example, human and dog 314 infections by Dirofilaria nematodes are becoming more frequent in Northern Europe with 315 increasing summer warming that facilitates parasite incubation (Genchi et al. 2011). Recognition of 316 long lag times and the role of environmental changes in invader and parasite dynamics suggests 317 that we need to endorse the precautionary principle: one should assume that any invader and 318 pathogen has the potential for undesirable effects and that lengthy periods of seemingly 319 innocuous behaviour can be a poor predictor of how these organisms will behave in the future 320 (Crooks 2005). 321 322 Hypotheses explaining biological invasions and analogues to epidemics 323 Invasion biology has formulated and tested several hypotheses on why some non-native species 324 go through the stages of the invasion process, whereas others do not (e.g. Catford et al. 2009, 325 Jeschke and Heger 2018). Invasions are influenced by many factors, and these can be grouped into 326 five categories related to propagule pressure, organism traits, biotic interactions, eco-evolutionary 327 experience and recipient system characteristics (Enders et al. 2020). Each of these five categories 328 16 agriculture has facilitated the emergence of zoonotic agents and the spread of non-native pests 602 (Hulme 2020). 603 Unfortunately, whereas some aspects of public health ensuing from the introduction of human 604 pathogens and vector mosquitoes are managed, others, including potential vertebrate hosts and 605 ectoparasites, are less effectively addressed. Thus, an integrated approach to biosecurity that 606 addresses both species invasions and emerging infectious pathogens appears necessary. The 607 research, stakeholder and policymaker communities are rapidly beginning to understand the need 608 for better integration between disciplines. This includes initiatives such as One Health, which has a 609 goal to achieve optimal public health outcomes by monitoring and managing the interactions 610 between humans, animals, and their environment. Likewise, the Planetary Health Alliance seeks to 611 determine the human health consequences of human-caused disruptions of Earth’s natural 612 systems (Myers 2017). Nevertheless, neither One Health nor Planetary Health adequately captures 613 the underlying nature of invasions by human pathogens and their relationship with invasive non-614 native species. A more robust framework can be provided by the concept of One Biosecurity that, 615 in addition to increasing the synergies between human health and invasion science, aims to 616 refocus discussions towards practical tools and policies for preventing, eradicating and containing 617 biosecurity risks (Hulme 2020). The possibility of implementing the One Biosecurity concept has 618 been further elaborated to highlight how international public health policy can be adapted to 619 address much wider biosecurity risks stemming from invasive non-native pathogens, plants and 620 animals through developing new risk assessment tools that look beyond national borders towards 621 biosecurity risks of international concern; a stronger regulatory instrument to address biosecurity 622 threats at a worldwide scale; and the establishment of an international biosecurity convention 623 responsible for biosecurity governance (Hulme 2021). 624 Management actions. Management actions against epidemics follow the same steps as in 625 invasions: prevention, early detection, containment, control and eradication, and long-term 626 management (Dunn and Hatcher 2015, Robertson et al. 2020). Many countries have in place early 627 detection and rapid response systems, but the administrations in charge are usually not the same, 628 with public health institutions to prevent epidemics, separated from environmental bodies to 629 avert invasions. Successful management prospects decrease with time elapsed since the onset of 630 the invasion or pathogen emergence (Fig. 4). Due to the rapid range expansion of many invasive 631 species and pathogens, the window of opportunity for early detection and response is often very 632 short. Control is usually the action that takes most of the time and effort. Eradication is difficult to 633 achieve except in small areas or remote areas and if actions start at early stages of invasion (Pluess 634 et al. 2012). Prompt detection and control of emerging pathogens requires proper tracing of 635 infected hosts independently of whether they are symptomatic or not. Eradication is very difficult 636 when infected hosts are widespread, and often requires vaccination of 50-90 % of the population 637 depending on how contagious the pathogen might be to achieve herd immunity. A major 638 difference between an epidemic and an invasion is that when an epidemic takes place at a given 639 locality, all of these management strategies might need to be set up simultaneously. That is, within 640 a human population, different groups of people need to take different precautions or treatment 641 measures, depending on their exposure to the pathogen. In a pandemic, all management practices 642 need to be scaled up at once, both within and among populations of different regions. Conversely, 643 since the rate of expansion of an invader follows a slower pace than that of a pathogen (Fig. 5), its 644 management is more aligned with the stage of invasion than in epidemics. 645 646 Risk assessments. To inform managers and policy makers, research on biological invasions 647 17 provides semi-quantitative risk assessment tools to identify and prioritize species likely to become 648 invasive and cause damage. Risk assessments also seek to identify the most susceptible habitats to 649 invasion by a particular, or several, invasive species, through consideration of both species traits 650 and recipient ecosystem characteristics. In human epidemics, the focus of the risk analysis is 651 primarily on a particular pathogen, albeit multiple hosts, and the risk of contagion and spread, is 652 based on the traits of the pathogen and the demographic characteristics (e.g. gender, age, activity) 653 of the receptive human host population. Spatially explicit risk assessments of invasion are very 654 common and mainly rely on land-use and climate correlates between the native and the 655 introduced area. These risk analyses have been implemented in vector-borne pathogens but could 656 also be conducted for emerging pathogens albeit human population density and movement 657 patterns seem to be better predictors of disease vulnerability than environmental characteristics 658 (Jones et al. 2008). Models such as EFBI, that view ecosystems as hosts that differ in exposure, 659 susceptibility, infectivity and rates of recovery could potentially be a basis for parallel risks 660 assessments for invasive species and human pathogens since they explicitly link the transmission 661 of invasive species between ecosystems and rather than derive an arbitrary score or probability on 662 invasion likelihood, risk assessment tools could be designed to estimate R0 (Hulme et al. 2020). 663 The evaluation of the impacts caused by epidemics focuses on the rates of infected people and 664 fatalities, which are used to compare pathogens, regions, and management responses. However, 665 as in invasions, which consequences extend beyond environmental impacts, the consequences of 666 epidemics extend beyond health, both having socioeconomic impacts (Dobson et al. 2020). 667 Attempts to quantify socioeconomic impacts in monetary terms are unlikely to provide a useful 668 basis for evaluating and comparing impacts of invasive species and pathogens, because they are 669 extremely difficult to estimate and may neglect important aspects of human well-being. In 670 invasions, there are many standardized impact assessment protocols that allow objective and 671 transparent ways to rank and identify the worst invasive species. Notably, the Socio-Economic 672 Impact Classification of Alien Taxa (SEICAT, Bacher et al. 2017) classifies invasive species based on 673 the magnitude of their impacts on human well-being, based on the capability approach from 674 welfare economics (Robeyns 2011). In SEICAT, impacts are assigned to one of five levels – from 675 minimal concern to massive – according to semi-quantitative scenarios that describe the severity 676 of the impacts on security, material and non-material assets, health, freedom of choice and action, 677 and social, spiritual and cultural relations. All these impacts apply to any epidemic and thus SEICAT 678 could be used to summarize and compare their impacts at national, regional or global scales. 679 Conclusions 680 In recent decades, we have witnessed how human activities that are poorly regulated can drive 681 harmful invasive species and pathogen outbreaks (Perrings et al. 2002, Stein 2020). The 682 epidemiology of human pathogens and invasion biology share many of the same mechanisms, 683 phenomena and challenges, but also potential solutions (Table 3). Global trade and travel are 684 prime causes for the introduction of invasive species and pathogens, for invasive vertebrate 685 reservoirs and for invasive insect vectors. Even the patterns and dynamics of spread of re-686 emerging “native” diseases, such as Ebola in West Africa and dengue in Southeast Asia, share 687 similarities to those of invasive species. Many of the pathogens that cause these diseases can 688 quickly become pandemics and then go through the same stages as invasive species. Much theory 689 and empirical insights gained in invasion biology can be extended to the study of emerging 690 pathogens; similarly, invasion biology can immensely benefit from insights gained on the study of 691 emerging human infectious pathogens. The amount and quality of the data collected on human 692 18 infectious pathogens is undoubtedly much more refined than that available for other invasive 693 species, as has been shown for SARS-CoV-2 (Bertelsmeier and Ollier 2020). 694 A cross-disciplinary perspective on infectious diseases and invasion biology could advance both 695 fields. We advocate for an One Biosecurity (sensu Hulme 2020, 2021) approach to: (1) develop a 696 unified frameworks for studying the pathways of introduction and the consequences of eco-697 evolutionary novelty; (2) compile and harmonize databases and information systems on major 698 invasions and epidemics; (3) share predictive modelling skills of the spread and impacts of invasive 699 species based not only on species traits but also on environmental characteristics; and (4) discuss 700 institutional approaches and protocols in horizon scanning, risk assessments, systematic 701 surveillance and monitoring of invasions and epidemics. 702 Undoubtedly, globalization and the movement of organisms across biogeographic barriers is not 703 only threatening biodiversity but also directly affecting human well-being through an array of new 704 emerging infectious threats. Invasion biology has accumulated over recent decades many insights 705 that could help improve the way we deal with these pathogens and the diseases they cause, but 706 crossing this disciplinary bridge requires more tangible collaborations and concrete policy 707 initiatives. Scientists, governments and institutions should promote the cross-disciplinary 708 approach to further advance in understanding the increasing threats of these novel entities and 709 improve prevention and response measurements. 710 Acknowledgements 711 We gratefully acknowledge comments from R. Mack and two anonymous reviewers to a previous 712 version of this manuscript. This study was supported by the 2017-2018 Belmont Forum—713 BiodivERsA International joint call projects InvasiBES and AlienScenarios under the BiodivScen 714 ERA-Net COFUND program and with the following funding organizations: the Spanish Ministry of 715 Science and Innovation (PCI2018-092986 and PCI2018-092939, MCI/AEI/FEDER), the German 716 Federal Ministry of Education and Research BMBF (01LC1803A), and the Austrian Science 717 Foundation FWF (I 4011-B32). AP was funded by CONICYT PIA AFB170008; AMD by NERC 718 (NE/P016766/1); EGD by PID2019-111109RB-I00 and RyC grant RYC-2013-13445; AR by NSERC 719 RGPIN-2016-03918; BG by RyC grant RYC2018-025160-I. 720 721 References 722 Alcami A, Koszinowski UH. 2000. Viral mechanisms of immune evasion. Trends in Microbiology 8: 723 410–418. 724 Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, 725 Daszak P. 2017. Global hotspots and correlates of emerging zoonotic diseases. 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Human emerging diseases can be caused directly by invasive pathogens, by pathogens 1193 transported by invasive vectors or reservoirs, or facilitated by invasive species not directly involved 1194 in the life cycle or transportation of the pathogen, but rather promoting the presence and 1195 abundance of its vectors and reservoirs. See examples in Table 1. 1196 Figure 2. Interplay between biological invasions and human emerging infectious diseases. 1197 Pathogen transmission can be within invasive species (left), within native or livestock species (right) 1198 and across invasive and native species. Dashed arrows indicate pathogen transmission to humans 1199 within a population (small circle) or globally (large circle). 1200 Figure 3. Cumulative number of publications on biological invasions, human epidemics and the 1201 combination of both topics according to the Web of Science from 1800 until 2020. Notice that the 1202 y-axis is in log scale. The search term for human epidemics was “human epidemics” whereas for 1203 biological invasions, the search term was “ecological invasions”. This term was more specific to 1204 retrieve all studies on that topic, while excluding non-topic studies (e.g. cancer research, 1205 pharmacology and biomaterial science). 1206 Figure 4. Comparing the stages of biological invasions and human epidemic (adapted from 1207 Woolhouse and Gaunt 2007, Blackburn et al. 2011, Hatcher et al. 2012, Jeschke et al. 2013), and 1208 possible management actions at these stages (adapted from Dunn and Hatcher 2015, Robertson et 1209 al. 2020). Pathogens that emerge and cause an epidemic anywhere on the globe can be 1210 transported and spread globally leading to a pandemic in the worst case (dotted arrow). Bent 1211 arrows indicate potential positions of zoonotic pathogen interspecific spillover. 1212 Figure 5. Density plot showing the frequency of observed radial spread rates (log scale) for 1213 different pathogens and invasive taxonomic groups. The height of each density curve indicates the 1214 relative number of data points, normalized to 1. Numbers at the right indicate the median rate of 1215 spread for the group. Figure created with packages ggplot2 and ggridges in R v. 4.0.0. Raw data 1216 extracted from: (Smal and Fairley 1984, van den Bosch et al. 1992, Holmes 1993, Teangana et al. 1217 2000, McCallum et al. 2003, Phillips et al. 2007, Pioz et al. 2011, Fraser et al. 2015, Zinszer et al. 1218 2015, 2017, Evans 2016, Roques et al. 2016, Horvitz et al. 2017, Hadfield et al. 2019). 1219 1220 33 Box 1. Definitions of terms and concepts as used in this paper 1221 Emerging infectious disease: an infectious disease that appears in a human population for the first 1222 time or has existed previously but is rapidly increasing in incidence, impact or geographic range 1223 (http://www.emro.who.int/health-topics/emerging-diseases/index.html). 1224 Epidemic: a disease event affecting many persons at the same time, and spreading from person to 1225 person in a locality or region during a specific period of time 1226 (https://www.who.int/csr/disease/swineflu/frequently_asked_questions/pandemic/en/). 1227 Invasive species: a non-native introduced species that form self-sustaining populations and spread 1228 rapidly from the sites of introduction (Blackburn et al. 2011). 1229 Invasiveness: intrinsic characteristics of a non-native species to invade outside its region of origin 1230 (Lonsdale 1999). 1231 Invasibility: susceptibility of an ecosystem to be invaded. It depends on the biotic and abiotic 1232 characteristics of the recipient ecosystem (Lonsdale 1999). 1233 Non-native species: an introduced species transported intentionally or unintentionally to a new 1234 region by humans (Blackburn et al. 2011). 1235 One Biosecurity: an interdisciplinary approach to biosecurity policy and research that builds on 1236 the interconnections between human, animal, plant, and environmental health to effectively 1237 prevent and mitigate the impacts of invasive alien species (Hulme 2021). 1238 One Health: cross-sectoral approach to achieve optimal public health outcomes by monitoring, 1239 managing and investigating the interactions between humans, animals, and their environments 1240 (Ogden et al. 2019). 1241 Outbreak: the occurrence of more infection cases than expected in a particular population, in a 1242 specific geographical area and in a specified period (http://www.emro.who.int/health1243 topics/disease-outbreaks/index.html). 1244 Pandemic: an epidemic occurring worldwide, or over a very wide area, crossing international 1245 boundaries and usually affecting a large number of people 1246 (https://www.who.int/csr/disease/swineflu/frequently_asked_questions/pandemic/en/) 1247 Pathogen pressure: amount of pathogen available to the human host at a given point in space and 1248 time (Plowright et al. 2017). 1249 Reservoir: an animal species that hosts a pathogen, typically without being harmed, and is the 1250 source of infection to other host species (Rabitsch et al. 2017). 1251 Spillover: transmission of a pathogen from a reservoir to a novel susceptible host (Rabitsch et al. 1252 2017). 1253 Time lag: period between the introduction of a non-native species and its establishment in the 1254 new range. In the broad sense, it can be applied to the time required to overcome any phase of 1255 the invasion process (Crooks 2005). 1256 34 Vector: a species, typically but not always an arthropod, that carries and transmits a pathogen to 1257 another species (Rabitsch et al. 2017). 1258 Virulence: ability of a microorganism to cause disease. It depends on characteristics of the 1259 pathogen and the host (Horrocks et al. 2011). 1260 Zoonosis: a disease causing pathogen that is transmitted between vertebrate animals (wildlife, 1261 livestock or domestic animals) and humans (Rabitsch et al. 2017). 1262 1263 35 Tables 1264 Table 1. Species from the IUCN list “100 of the World’s Worst Invasive Alien Species” (Lowe et al. 1265 2000) that can transmit pathogens to humans or are themselves pathogens. The introduction 1266 pathways (according to the Convention of Biological Diversity) and impact types (A: damage 1267 human activities such as to agriculture, forestry, livestock or infrastructures; B: biodiversity; H: 1268 human health) are indicated. 1269 Invasive species Pathogens (diseases) Transmission Pathways Impacts Acridotheres tristis, common myna Ornithonyssus bursa and Dermanyssus gallinae (dermatitis, skin inflammation, severe irritation and rashes, asthma) Their droppings can spread psittacosis, ornithosis, salmonelosis and arboviruses. Reservoir Intentional/ Escape from confinement: Zoo, Pet trade Intentional/ Release in nature: Fauna “improvement” A, B, H Aedes albopictus, tiger mosquito Flavivirus spp. (e.g. West Nile, dengue fever), Dilofilaria immitis (filariasis) Vector Unintentional/ Transportstowaway: Vehicles H Achatina fulica, Giant African land snail Metastrongylus spp., Angiostrongulus cantonensis and A. costaricensis (pulmonary metastrongylosis and eosinophilic meningoencephalitis) Reservoir Intentional/Escape from confinement: Pet, Aquarium and terrarium species, Research, Horticulture, Live food H, A Anopheles quadrimaculatu, mosquito Plasmodium spp. (malaria), West Nile virus (meningoencephalitis) Vector Unintentional/ Transportstowaway: Vehicles H Eichhornia crassipes, water hyacinth Plasmodium spp. (malaria) transmitted by Annopheline mosquitoes Invasive facilitator (habitat for vector) Intentional/ Escape from confinement: Aquarium species A, B, H Eriocheir sinensis, Chinese mitten crab Paragonimus westermanii (human lung fluke parasite), Reservoir Intentional/ Escape from confinement: Aquaculture, Aquarium species. A, B, H 36 Unintentional/ Transportstowaway: Shipboat ballast water, Ship-boat hull fouling Euglandina rosea, rosy wolf snail Angiostrongylus cantonensis (pulmonary metastrongylosis and eosinophilic meningoencephalitis) Reservoir Intentional/ Release in nature: Biological control B, H Herpestes javanicus, small Indian mongoose Leptospira interrogans (Weil’s disease), Lyssavirus (rabies) Reservoir Intentional/ Release in nature: Biological control B, H Lantana camara, lantana shrub Tripanosoma spp. (sleeping sickness) transmited by Glossina spp., tse tse fly Invasive facilitator (habitat for vector) Intentional/ Escape from confinement: Horticulture A, B, H Macaca fascicularis, crab-eating macaca Macacine herpesvirus 1 (herpes B), Lyssavirus (rabies) Reservoir Intentional/ Escape from confinement: Live food, Research A, B, H Mus musculus, house mouse Yersinia pestis (bubonic plague), Salmonella spp. (salmonelosis) Reservoir Unintentional/ Transportstowaway: Container, bulk A, B, H Rattus rattus, black rat Leptospira interrogans (Weil’s disease), Yersinia pestis (bubonic plague) Reservoir Unintentional/ Transportstowaway: Container, bulk A, B, H Sturnus vulgaris, starling Chlamydophila psittaci (psittacosis) Reservoir Intentional/ Release in nature: Biological control, Hunting, Fauna “improvement” A, H 37 Sus scrofa, feral pig Leptospira interrogans (Weil’s disease) Reservoir Intentional/ Release in nature: Hunting A, B, H Trachemys scripta elegans, red eared slider turtle Salmonella spp. (salmonelosis) Reservoir Intentional/ Escape from confinement: Aquarium and terrarium species A, B, H Vulpes vulpes, red fox Possible role in Lyssavirus (rabies) transmision Reservoir Intentional/ Release in nature: Hunting A, B, H 1270 1271 1272 38 Table 2. Differences and common challenges associated with the forecasting of biological invasions 1273 and human epidemics with indications of the potential for collaboration and cross-fertilization 1274 across disciplines. 1275 Biological invasions Human epidemics Potential crossfertilization across disciplines Data used Geo-referenced species occurrence Rarely, abundance data Number of infected individuals Information rarely georeferenced Common monitoring systems and data platforms Indicators (developed to follow an outbreak) Likelihood of species presence (suitability) Number of non-native species R0, likelihood of exponential spread Correlation between disease and invasion indicators Models Mostly spatially, nichebased, e.g. Species Distribution Models (SDMs) Dynamic, biologybased e.g. Susceptible Immune Recovered (SIR) Sharing modelling tools and advances to reduce uncertainty Scales Regional to global Years/decades Local to regional Rarely global Weeks/months Automatically updated platforms to follow an outbreak Critical factors (ordered) Climate Environmental conditions Human activities (e.g. transport, land-use) Biological (e.g. dispersal) Biological (e.g. transmissibility) Human activities (e.g. transport) Human behavior (e.g. sociability) Management (e.g. medical and nonmedical actions) Share environmental and human data for modelling New sources of human-related data (e.g. mobile phones, trade flows) Approaches Exploratory Climate change scenarios Management scenarios Intervention scenarios Common scenario frameworks and workflows Common challenges Data quality and quantity Modelling of complex systems under imperfect detection Incorporating human activities and behaviors Anticipating alternative policy and management scenarios High intrinsic uncertainty associated to exponential processes Traceability of origin and expansion of pathogen/invader Lag phases (e.g. between introduction and impact, between management and effective mitigation) 39 Anticipating the next biological threat based on transmissibility/spread and potential impacts 1276 40 Table 3. Comparison of main features and established concepts of biological invasions with human 1277 epidemics. 1278 Feature Biological invasions Human epidemics References Biogeograph ic and evolutionary origin Non-native species from a region where they could not be dispersed without human agency Non-native pathogens dispersed directly or indirectly by humans or emerging native pathogens. Crossing a species barrier rather than a biogeographic barrier (Jones et al. 2008, Pyšek et al. 2017) Routes of dispersal Pathways Intentional: release and escape Unintentional: contaminant, stowaway, corridor and unaided Routes of infection Unintentional: vector borne, zoonotic, human contact, indirect contact by ingestion or the environment Also intentional: historical cases during colonization of new territories, bioterrorism and anthrax mailing (Wolfe et al. 2007, Hulme et al. 2008, Saul et al. 2017) Founder populations Repeated introductions from several populations, genetically diverse (admixtures) Few introductions from a single or few populations Stages Transport, introduction, establishment, spread Exposure, infection, transmission, epidemic spread; zoonotic spillover (Woolhouse and Gaunt 2007, Blackburn et al. 2011, Jeschke et al. 2013) Spread rates and time lags 0.1-102 km/yr Years-decades 103-104 km/yr Days-decades (Kowarik 1995, McCallum et al. 2003) See Figure 4 41 Main studied causes of non-native species performance and impact Traits of the organism (invasiveness), biotic and abiotic characteristics of the recipient ecosystem (invasibility) and the intensity and frequency of introduced individuals (propagule pressure) Traits of the organism (pathogenicity), host age, genetics, physiology, immunity and people behavior (Lonsdale 1999, Mack et al. 2000, Enders et al. 2020) Forecasting models’ focus and explanatory variables On the invasive species. Environmental and proxies for propagule pressure as explanatory variables On infected people (not the pathogen). Human demographics including movement and pathogen transmission as explanatory variables See Table 2 Traditional impact focus Biodiversity, environment, agriculture and farming Medical, public health (Jeschke 2014, Vilà and Hulme 2016) Traditionally involved managemen t sectors Environment, agriculture and farming, veterinary, water resources, trading Public health, food, foreign affairs, traveling, veterinary, water resources (Ogden et al. 2019) 1279 1280 1281