Understanding invasion success of Pseudorasbora parva in the Qinghai-Tibetan Plateau: Insights from life-history and environmental filters

https://doi.org/10.1016/j.scitotenv.2019.133739Get rights and content

Highlights

  • Mechanisms of invasion success of topmouth gudgeon were explored in the Tibetan Plateau.

  • Invasive and native populations had distinct life history strategies.

  • Sex-specific life history plasticity along an elevational gradient was observed.

  • Important environmental correlates of occurrence patterns were identified.

Abstract

Understanding mechanisms of fish invasion success is crucial to controlling existing invasions and preventing potential future spread. Despite considerable advances in explaining successful fish invasions, little is known about how non-native fish successfully invade alpine freshwater ecosystems. Here, we explore the role of fish life history and environmental factors in contributing to invasion success of Pseudorasbora parva on the Qinghai-Tibet Plateau. We compared life history trait differences between native populations in lowland China with introduced populations in lowland Europe and the high elevation Qinghai-Tibet Plateau. Linear mixed-effects models were used to analyse life-history trait variation across elevation gradients. A random forest model was developed to identify the key environmental filters influencing P. parva invasion success. Life history characteristics differed substantially between native and introduced populations. Compared with native Chinese populations, introduced populations in lowland Europe had smaller body size, higher fecundity, smaller oocytes and earlier maturation. Introduced populations in the Qinghai-Tibet Plateau had smaller body size, lower fecundity, smaller oocytes and later maturation compared with native populations. 1-Year-Length and fecundity in all age classes of females significantly increased with increasing elevation. 2-Year-Length and 3-Year-Length of male significantly increased while maximal longevity and length at first maturity were significantly decreased with the elevation gradient. Habitat type, annual mean temperature, elevation, annual precipitation and precipitation seasonality, were the 5 most important predictors for the occurrence of the P. parva. Our study indicates that invasive P. parva adopt different life history strategies on the plateau compared with invasive populations at low elevations, highlighting that more studies are required for a better understanding of biological invasion under extreme conditions. Considering the ongoing hydrologic alteration and climate change, our study also highlighted that P. parva may expand their distribution range in the future on the Qinghai-Tibet Plateau.

Introduction

Non-native fishes pose a considerable threat to freshwater ecosystems around the world and can have catastrophic ecological and economic consequences (Vitule et al., 2009; Cucherousset and Olden, 2011; Piria et al., 2018). Non-native fish disrupt native fish communities through several potential mechanisms (Cucherousset and Olden, 2011), including hybridization and introgression (Muhlfeld et al., 2017), herbivory (Miller and Provenza, 2007), competition (Marras et al., 2015), predation (Correa et al., 2012), disease transmission and parasitism (Poulin et al., 2011), changes in food webs (Britton et al., 2010), and habitat alteration (Koehn, 2004). These processes may alter community structure, ecosystem functioning and provision of ecosystem services for people (Vilà et al., 2010; Cucherousset and Olden, 2011). Considering the pervasive ecological and economic impacts of non-native fishes on freshwater ecosystems, an understanding of the mechanisms of fish invasion success are needed to inform management of existing invasions and prevent future invasions (García-Berthou, 2007; Aschonitis et al., 2018).

Many biotic and abiotic factors have been proposed as potential determinants of invasion success of fish (Kennard et al., 2005; Moyle and Marchetti, 2006; Fitzgerald et al., 2016; Gavioli et al., 2018; Wellband et al., 2018). Although these factors may be species- and/or region-specific, life history traits of the invasive species and environmental characteristics of the invaded system are recognized as important filters for the outcome of the invasion (Grabowska and Przybylski, 2015; Howeth et al., 2016). Several theories about life history have been used to explain the successful invasion of fishes, such as r-and K-selection (Pianka, 1970), life history theory (Stearns, 1992) and alternative ontogenies and developmental plasticity (Vilizzi and Kováč, 2014). For example, life-history theory predicts that invasive populations will display fast (opportunistic) strategies with early maturity, high reproductive investment, and a short lifespan (Stearns, 1992; Winemiller and Rose, 1992). Life-history traits have also been widely used as predictors of fish invasion success and species invasiveness (Olden et al., 2006). In addition, examination of intra-specific variation in life-history traits of invasive species at large spatial scales (e.g. along latitudinal or salinity gradients) can provide insight into mechanisms influencing potential invasiveness of species and environmental factors limiting their spread (e.g. Alcaraz and Garcia-Berthou, 2007; Benejam et al., 2009; Carmona-Catot et al., 2011). For instance, invasive mosquitofish (Gambusia holbrooki) populations in lower latitudes allocated more energy to reproduction and had a lower condition (Carmona-Catot et al., 2011). In addition, mosquitofish females exhibited earlier maturation, higher reproductive investment and a reduced condition and density along a gradient of increasing salinity (Alcaraz and Garcia-Berthou, 2007). Understanding how life history trait characteristics vary along environmental gradients can also be used to predict shifts in distributions in response to global environment changes (Benejam et al., 2009). In terms of environment, Moyle and Light (1996) highlight the important role of abiotic factors in determining fish invasion success and suggest in some systems that, if abiotic factors are suitable for an introduced species, it will invade successfully regardless of biotic factors.

Despite these advances in general understanding of mechanisms of invasion success, evidence from ecosystems exposed to extreme environmental conditions, especially plateau or mountain freshwater ecosystems, remains limited. Alpine ecosystems, which can be considered as bioclimatic and biogeographic islands (Burke, 2003), are regarded as inherently more susceptible than other ecosystems to fish invasion (Grêt-Regamey et al., 2012). This environment typically supports a high concentration of endemic aquatic species within a small geographical range and which are particularly vulnerable to the adverse effects of invasion (McNeely et al., 2009). However, the rate of fish invasion in these ecosystems is rising because of the increasing incidence of intentional and accidental introductions of non-native species, and because anthropogenic disturbance and climate change is likely to increase the inherent invasibility of these regions (Adams et al., 2001; Ilhéu et al., 2014).

The Qinghai-Tibetan Plateau (Q-T Plateau) in China provides an excellent model system to improve our ecological understanding of fish invasion success in alpine freshwater ecosystems. At least 15 non-native fish species have successfully established on the Q-T Plateau, the most wide-spread and abundant of which is the topmouth gudgeon, Pseudorasbora parva. This small freshwater cyprinid species is native to eastern Asia, including lowland China, but has spread widely throughout central Asia, Europe and north Africa. The invasion success of this species has been attributed to its high plasticity of life history traits and broad environmental tolerances (Gozlan et al., 2010; Záhorská et al., 2014).

The aim of our study was to explore the role of life history and environmental filters in influencing invasion success of P. parva in the Q-T Plateau. Our specific objectives were to: (1) Compare trait characteristics of P. parva from native and introduced populations in China and Europe to clarify how life history plasticity may contribute to invasion success of this species in the Qinghai-Tibet Plateau; (2) quantify trait variation of P. parva along an altitudinal gradient in Tibetan rivers to elucidate how trait plasticity in P. parva facilitates invasion and spread in the plateau; (3) quantify potential environmental determinants of invasion success in Tibetan rivers to identify which environmental filters are important for determining the P. parva occurrence in the Qinghai-Tibet Plateau. We expect that our study will contribute to a broader understanding of the mechanism for fish invasion success in alpine freshwater ecosystems.

Section snippets

Study area and focal species

The Q-T Plateau, often referred to as the ‘Third Pole’, is the highest and largest plateau on Earth, covering about 2.5 million km2 with an average elevation of 4000 m above sea level (Wu, 2001; Qiu, 2008). The Q-T Plateau is the source of some major rivers, such as the Yangtze, Yellow River and Yarlung Zangbo River, and is known as the “water tower of Asia” (J. Xu et al., 2009). Aquatic biota in the Q-T Plateau are characterized as highly specialised and of low diversity (Hamerlik and

Comparison of traits from native and introduced populations in China and Europe

Spatial differences in the four morphology and life history traits were observed between invasive populations of P. parva from the Q-T plateau, lowland Europe, and native populations in lowland China. Native Chinese (p = 0.059, marginally significant) and invasive European populations (p = 0.082, marginally significant) from low elevations had larger maximal length than high elevation populations from the Q-T plateau (Fig. 2a). In contrast, fish from the Q-T plateau were larger at first

Variation in traits from native and introduced populations in China and Europe

Plasticity in life-history traits has been recognized as an important advantage of invasive species, which allow them to optimize life history traits in response to environmental conditions of colonized habitats and play an essential role in invasion success (Chun et al., 2007; Valiente et al., 2010). Consistent with this assertion, invasive populations of P. parva at low elevations in Europe and extremely high elevations on the Q-T Plateau exhibit different biological trait characteristics

Acknowledgements

This research was financially supported by the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (Grant nos. 2019QZKK0501; 2019QZKK0304) and the National Natural Science Foundation of China (Grant no. 31372189). We wish to thank Mr. Ren Zhu, Heying Sun and Chaojun Wei for their help in field work.

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