Growth and Reproduction of the Nonnative Icefish
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Journal of Applied Ichthyology J. Appl. Ichthyol. 30 (2014), 862–869 Received: February 7, 2013 © 2014 Blackwell Verlag GmbH Accepted: March 11, 2014 ISSN 0175–8659 doi: 10.1111/jai.12475 Growth and reproduction of the non-native icefish Neosalanx taihuensis Chen, 1956 (Salangidae) in a plateau lake, southwestern China By F.-Y. Zhu1,2, S.-W. Ye1, Z.-J. Li1, T.-L. Zhang1, J. Yuan1, Z.-Q. Guo1,2, J.-F. Tang1,2 and J.-S. Liu1 1State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan, Hubei, China; 2University of the Chinese Academy of Sciences, Beijing, China Summary their influence on fish colonization in the new environment Growth, reproduction and abundance traits of the invasive remains poorly understood. For example, Rosecchi et al. icefish Neosalanx taihuensis Chen, 1956 were investigated (2001) showed that both gudgeon Gobio gobio and Asian monthly from July 2009 to May 2011 in Lake Erhai on the topmouth gudgeon Pseudorasbora parva could be classified Yunnan-Guizhou Plateau, south-western China, in order to as opportunists in southern France. Differences observed in explore the changes in life-history traits after translocation. their invasive success could be explained by the wider ecolog- The results indicated that the icefish exhibited obvious plas- ical and physiological tolerance and phenotypic plasticity of ticity in growth and reproduction traits. Growth of the fish the gudgeons. High levels of life-history plasticity also seem in Lake Erhai was faster than that in native waters and in to contribute greatly to the invasive success of Iberian pump- other translocated reservoirs. By fitting the von Bertalanffy kinseed Lepomis gibbosus on the Iberian Peninsula, which growth model to the data, it was estimated that icefish obtain adopted a more ‘opportunistic’ life-history strategy than its native counterparts (Fox et al., 2007). Grabowska et al. an asymptotic size of 96.12 mm, a K of 1.61, and a t0 of -0.26; the calculated overall growth performance index φ0 (2011) observed advanced maturation of females and an was 4.17. The strategy of reproduction changed from multi- extended spawning season in Amur sleeper Perccottus glenii ple- to single-spawning. The spawning period was from in the Wloclawski Reservoir, Poland, at a cost of slower October to December with the absolute and relative fecundi- growth of older age classes. This flexible strategy has made ties of 1250 Æ 169 eggs per ind and 2557 Æ 245 eggs per g, the Amur sleeper one of the most invasive fish species in respectively. Plasticity in icefish growth and reproduction in eastern and central Europe. Consequently, it can be hypothe- Lake Erhai greatly facilitated its population establishment, sized that the success of an invasive species can be dependent making it one of the most abundant fish species. The icefish on the plasticity of its life-history traits. invasion in the lake may be one of the reasons for the The icefish Neosalanx taihuensis Chen, 1956 (family: Salan- decrease or extinction of native fish species populations, and gidae, subfamily: Neosalanginae) is a small zooplanktivorous some measures for the control of this invasive fish are sug- fish endemic to China and restricted to large freshwater sys- gested. tems in the middle and lower reaches of the Yangtze River (Xie and Xie, 1997). Due to its commercial importance, the icefish has been introduced into a number of lakes and reser- Introduction voirs in most areas of China for fishery purposes (Wang The invasion of non-native fishes is one of the main causes et al., 2002; Liu et al., 2009). It has established relatively sta- for the decline in native freshwater fish diversity worldwide ble populations in most of these water bodies, although the (Lodge, 1993; Mills et al., 1994). Of growing concern to environmental factors fluctuated (Wang et al., 2005). In freshwater ecologists is the necessity to predict the risk of some water bodies the icefish has even become dominant. establishment or invasion of a given introduced species. Life- Despite its wide translocation and invasion, there are still history traits of non-native fishes were correlated with their few published studies on its life history trait plasticity; most invasion success and adaptation to environmental conditions of the previous research focused on fishery utilization in the (Rosecchi et al., 2001; Peterson, 2003). Therefore, life-history lower and middle Yangtze River basin (Liu et al., 2009). trait measurement is an effective approach to predict In the 1980s, N. taihuensis was introduced from Lake Tai- invasion success. A meta-analysis by Kulhanek et al. (2011) hu (a shallow lake in the lower reach of the Yangtze River) suggested that knowing the invasion history of a non-native to Lake Dianchi, and then to Lake Erhai, the largest two species can help predict the impact of its invasion in the lakes on the Yunnan-Guizhow Plateau, southwestern China. future. Unfortunately, detailed data for many invasive It soon established a population to become one of the domi- species in recipient systems are simply not available. nant species in Lake Erhai (Chen et al., 1998). Annual yield Phenotypic plasticity and flexibility in life-history traits in the past 10 years reached more than 800 tonnes, about seem to be typical attributes of successfully invasive fishes one-quarter of the total fish production of Lake Erhai (Fox et al., 2007; Novomeska and Kovac, 2009), although (unpublished data from the Lake Erhai Protection Agency). U.S. Copyright Clearance Centre Code Statement: 0175-8659/2014/3005–862$15.00/0 Growth and reproduction of icefish 863 With the successful establishment of the icefish population, some endangered native fish species populations (e.g. Cypri- nus longipectoralis, Cyprinus pellegrini, and Zacco taliensis, etc.) decreased further (Chen et al., 1998; Du and Li, 2001). We therefore hypothesized that icefish in Lake Erhai could be treated as an invasive species. Like most other successful invasive species, a flexible life-history strategy may facilitate its invasion. A study of life-history traits of the non-native icefish could explain the successful establishment of the fish and its impact on endangered fish species. The result may also be helpful for icefish population control in the new environment. Materials and methods Study site This study was carried out in Lake Erhai (99°320–100°270E, 25°250–26°160N), a plateau lake with an area of 250 km2 and an altitude of 1972 m. Maximum and average depths are 21.3 m and 10.5 m, respectively. Water temperatures in the lake range from 10.2°C to 22.6°C, with an annual mean tem- perature of 16.9°C. Seventeen native fish species have been recorded in Lake Erhai, including eight endemic species (Chu and Chen, 1990). Fig. 1. Neosalanx taihuensis sampling sites in three different areas of At least six endemic species populations declined or were Lake Erhai endangered in the 1970s with the invasion of two species of goby (Ctenogobius qiurinus and C. cliffordpopei) (Chen et al., 1998). Some conservation methods (such as seasonal fishing weight (W, 0.01 g). Statistical comparisons of length-weight banning and stock enhancement) were conducted since the relationships between males and females were performed 1970s, with some positive results. However, since the 1980s, the applying the 2-factor (month and sex) Analysis of Variance declining situation of native fish species deteriorated even fur- (ANOVA) (Zar, 1999); sex was determined through secondary ther with the introduction of the icefish, Neosalanx taihuensis, sex characters (Gong et al., 2009). Von Bertalanffy models which began in 1984. The yield attained 500 tonnes in 1991 and were applied to describe growth patterns in all specimens. increased yearly thereafter (Du and Li, 2001). Calculated length frequencies by month were used to fit the growth models through electronic length frequency analysis (ELEFAN) with FiSAT (FAO-ICLARM Stock Assessment Fish sampling Tools) (Gayanilo and Pauly, 1996). The von Bertalanffy Icefish samples were collected at three sites from south to growth function (VBGF) is: Lt = L∞(1–exp(–k(t–t0))), where north in the lake (Fig. 1) monthly from June 2009 to May Lt is total length (mm) at age t, L∞ is the asymptotic length 2011. A lift-net was used for the collection for about one (mm, computed as Lmax/0.95, where Lmax is the maximum hour after sunset. The opening gape of the lift-net was recorded length, according to Pauly, 1984; and Massimiliano 4m9 4.5 m with a 3 mm mesh size. The lift-net was set and Giancarlo, 2009), k is the rate at which the asymptotic horizontally, kept suspended in the water by lines held by length is approached, t is age in months, and t0 is the origin operators on two boats. In order to attract the icefish, a of the growth curve. 45 W lamp was installed over the lift-net. Five times during The phi-prime (φ0) parameter was calculated to compare each sampling the net was lifted quickly every 15 min. Cap- overall growth performance with the equation 0 tured fish were measured separately, immediately preserved φ = log10(k) + 2log10(L∞) (Pauly and Munro, 1984). with crushed ice in the field and stored at À20°C for later Fish mortality rates were computed with length-based analysis in the laboratory. analysis and von Bertalanffy growth parameters. Length- frequency data were used to calculate the total mortality rate (Z) by the Beverton & Holt model subprogram with the Data collection and analysis FiSAT. Natural mortality (M) was derived from the empiri- Total number and yield of icefish per net were counted as cal formula (Pauly, 1984): log M = À0.0066 – 0.279 log L∞+ catch per unit effort (CPUE) as an index of relative 0.6543log k + 0.463log T, where L∞ is the asymptotic length abundance.