Growth and Reproduction of the Nonnative Icefish

Home , Lake Tai

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 169 eggs per ind and 2557 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 temperature 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 20°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 = 0.0066 – 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. Data from each net at each site were treated as measured in total length, k is the VBGF growth constant, replicates. and T is the mean annual habitat temperature (16.9°C). In the laboratory, icefish were measured for total length Fishing mortality (F) was then obtained by subtracting M (TL, 0.01 mm), standard length (SL, 0.01 mm) and body from Z. 864 F.-Y. Zhu et al.

Only adult females were used to assess reproductive traits. estimated as 1.83 per year, 1.22 per year and 0.61 per year, About 30 females were randomly selected from each monthly respectively. sampling for further treatments. The gonads of females were dissected out and weighed (Mg, 0.0001 g). The stages of development of the gonads were identified as immature (I), Reproduction developing (II), spawning-capable (III), actively spawning The stages of gonad development showed significant annual (IV) and regressing (V) stages using the criteria established cycle (Fig. 5). Between February and July most female by West (1990). The number of mature oocytes (NO), defined gonads were at stage I or stage II. This situation changed here as the total number of oocytes in the actively spawning rapidly in August, where more than 50% of female gonads stage gonads, was calculated to estimate the absolute fecun- developed into stage III, and about 10% into stage IV. Stage dity of each specimen. The relative NO (NRO) was calculated I and stage II were rarely detected from September to Janu- 1 from NRO = NOME , where ME is the eviscerated masses. ary of the next year, when this generation died out. The gonadosomatic index (GSI) was also calculated only for The absolute fecundity (NO SE) was 1250 169 eggs 1 females, based on the equation: GSI = 100 Mg ME , where per ind. The relative fecundity (NRO SE) was Mg is the weight of the gonads (West, 1990). 2557 245 eggs per g. The sagittal otolith of the icefish was used for age determi- Female GSIs were observed from July 2009 to May 2011, nation in days at the early stage of the life cycle. Daily age and the major peak occurred in September (Fig. 6). The data were used for breeding season presumption. The sagittal mean female GSI (NO SE) was 11.06 1.25 in September otoliths of 40 juveniles randomly sampled in February 2010 2009 and 10.13 0.93 in September 2010. There was a nota- and February 2011 were dissected out to confirm the breed- ble coincidence between GSI and water temperature. ing time. A single hatching experiment was also conducted Based on the hatching experiment, the hatching period at to confirm the breeding time in November. Fertilized eggs 15°C was 8–14 days. The peak of hatching happened on day were obtained from artificial insemination of the mature ice- 10. The daily ages of 40 randomly selected fry were counted fish. A total of 20 000 fertilized eggs were put into a tank on February 2nd through the daily ring of sectioned sagittal with 27-L water for hatching. Temperature was limited at otoliths. The mean daily age (NO SE) was 15 1°C, which is the mean water temperature of Lake 52.28 0.94 days, ranging from 41 to 68 days. Conse- Erhai in November. Incubation duration was counted when quently, the spawning period of icefish in Lake Erhai was 50% of the fertilized eggs hatched. back-calculated, i.e. from November to December, with the peak spawning time in late November.

Results Fish abundance Discussion A total of 96 nets of icefish were collected during the Growth pattern research period. There were significant differences (P < 0.05) Data in the literature showed that icefish growth parameters in CPUE among different months, with the CPUE showing varied considerably by geographic area (Table 3). A native remarkable seasonal fluctuation (Fig. 2), ranging from 3 to to Lake Wanghu in the middle reach of the Yangtze River, 507 ind/net/15 min, for a maximum in spring (May and the icefish had the highest k value but almost the lowest L∞, June) and minimum in winter (December and January). The represented high growth rate and almost the smallest adult yield of each net ranged from 0.59 to 100.27 g, reaching the body size (Yin et al., 1997). In introduced locations, the maximum in summer (July and August) and minimum in body size was bigger than its native population but grew rel- winter (January and February). atively slowly (Table 3). An exception was the icefish in the present study, which had almost the highest growth rate as well as the biggest adult body size (Table 3). The variation Growth, mortality and lifespan in growth parameters is commonly seen in widely distributed Some 2859 icefish individuals (552 juveniles, 569 males and fish species in native areas (Lobon-Cervi a et al., 1996) or in 1738 females) were measured for total length distribution newly-colonized waterbodies (Villeneuve et al., 2005), likely a (Table 1, Fig. 3). There were significant differences consequence of the discrepancy in climate, food resources, (P < 0.001) in monthly mean lengths and weights between density dependent factors, etc. (Grabowska et al., 2011). The male and female icefish based on the two-way Analysis of flexibility of growth parameters revealed a different adapta- variance (ANOVA); thus data for each sex were put into tion approach to variable environmental conditions (Rosec- FiSAT software separately for fitting the von Bertalanffy chi et al., 2001). In Lake Erhai, there is no predator of growth equation; juveniles were used for fitting the equation icefish (Chu and Chen, 1990); there are also few planktivo- of both sexes. The fitted growth parameters are shown in rous fish species in middle and upper water column that Table 2. Goodness of fit was assessed by visual appearance could compete with icefish for food (Chen et al., 1998; Du of the plotted data, and the growth lines (where each line and Li, 2001), except for the silver carp Hypophthalmichthys represents 1 generation) were obtained by ELEFAN (Fig. 4). moritrix and bighead carp Aristichthys nobilis, two carps Based on the VBGF parameters, the total mortality, that could not naturally breed in the lake (Xie and Chen, natural mortality, and the fishing mortality rates were 2001), as well as some juvenile native fish species that are Growth and reproduction of icefish 865

Fig. 2. Mean number (n = 5) and weight (n = 5) of catch per unit eﬀort (CPUE) of iceﬁsh, Lake Erhai, June 2009 to May 2011

Table 1 Total length of iceﬁsh in Lake Erhai, June 2009 to January 2011

Females Males

Time N Mean SE N Mean SE

Jun-09 315 52.11 0.43 49 52.49 0.92 Jul-09 238 51.67 0.38 87 54.31 0.47 Aug-09 256 54.80 0.30 110 53.83 0.42 Sep-09 31 56.07 0.70 15 54.09 1.50 Oct-09 128 61.17 0.57 43 57.07 0.93 Nov-09 17 67.64 2.43 8 62.05 4.21 Dec-09 40 69.81 2.41 9 63.18 3.53 Jan-10 3 72.42 2.89 18 66.65 3.04 Feb-10 6 70.45 4.19 5 68.68 4.75 Jun-10 102 49.90 0.44 3 50.29 1.65 Jul-10 142 51.14 0.46 36 53.58 0.45 Fig. 3. Growth pattern of icefish from Lake Erhai. Circles = means; Aug-10 151 57.74 0.56 49 56.55 0.77 vertical bars = 2SE above and below the means Sep-10 99 60.12 0.58 55 56.82 0.58 Oct-10 90 63.15 0.81 19 58.01 1.73 Nov-10 54 64.03 1.08 12 60.64 2.26 Dec-10 45 66.36 1.38 12 63.04 2.08 of fish to various environmental conditions (Ziliukiene_ and Jan-11 15 68.23 1.64 19 64.89 0.95 Ziliukas, 2010). In the present study, analyses of VBGF parameters and φ0 both revealed that the introduced icefish population in Lake Erhai showed obvious advantages in endangered or almost extinct. Therefore, the implication is growth performance compared to populations in the native that the faster growth and bigger size of the icefish in Lake and other colonized water bodies. These advantages clearly Erhai is an important adaptation in such a relaxed environ- characterize the ability of its populations and individuals to ment with no predation risk and a low competition level. adapt to the different conditions in Lake Erhai. The growth comparison of fish based on a single parame- The growth plasticity exhibited in different populations of ter k or L∞ has been found to be misleading (Kimura, 1980). icefish illustrates a flexible colonisation strategy. Rapid reac- The asymptotic length of fish growth generally increases with tion to environmental change is possible with a 1-year life- age, whereas the coefficient of the growth rate k decreases span and flexible growth pattern. This efficient use of climate (Zivkov et al., 1999). Thus Pauly and Munro (1984) pro- and food resource may be one of the reasons that give icefish posed indices of overall growth performance (φ0) for compar- a good adaptability to different conditions and to maintain a ison. The growth performance partly reflects the adaptability self-sustaining population in large areas. 866 F.-Y. Zhu et al.

Table 2 duced waters (Gong et al., 2009). In the native regions and Von Bertalanffy parameters for icefish, Lake Erhai, June 2009 to in all introduced waters, the icefish usually have multiple- May 2011 spawning periods: one major group spawns in spring and the Males Females Sexes combined minor group spawns in autumn. In addition, the relative fecundities in the native regions and other translocated areas n 2323 3486 4037 ranged from 1071 eggs per g to 1400 eggs per g (Yin et al., L∞ 89.15 96.12 96.12 1997; S. Gong et al., 1999; W. B. Gong et al., 2009), which k 1.61 1.31 1.61 were much lower than the value of 2557 eggs per g in Lake t0 0.26 0.32 –0.26 Z 2.99 2.04 1.83 Erhai. M 1.36 1.22 1.22 Multiple spawning has been considered an adaptation by F 1.63 0.82 0.61 fish to reduce the negative impacts of environmental varia- tions on reproduction success (Winemiller and Rose, 1992; Grabowska, 2005). Grabowska (2005) found that the racer Reproductive strategies goby Neogobius gymnotrachelus extended its breeding season The reproductive traits in the present study showed that ice- and bred more times after invading the Wloclawski Reser- fish have only one spawning period (from late autumn to voir, to adapt to the occasional occurrence of unfavourable early winter) in Lake Erhai. This is a significant difference conditions. Palacios et al. (1999) reported that wild shrimp both from its native populations in the middle and lower had higher mating and spawning frequencies compared to reaches of the Yangtze River, e.g. in Lake Hongze (Zhang pond-reared broodstock that lived in a stable environment, et al., 1982), Lake Poyang (Chen and Zhang, 1990), and but that fertilization and hatching rates were higher for Lake Taihu (Ni and Zhu, 2005), and also from other intro- pond-reared spawners. In Lake Erhai, there is no obvious

Fig. 4. Growth lines obtained by ELEFAN for males (black, n = 1121), females (gray, n = 2290) and combined sexes (n = 2859) of icefish in Lake Erhai. Juveniles were used for fitting the growth lines of both sexes Growth and reproduction of icefish 867

temperature and zooplankton biomass in the lake (Fig. 6). Hence, a multiple-spawning strategy could be less efficient than the single-spawning strategy in such a water body. The icefish did not need to spend all of their reproductive investment in both autumn and spring spawning (as the native and other introduced populations), but only in the autumn. This reproductive strategy maintains a large number of individuals with a low icefish population biomass during winter (Fig. 2). Hence the energy requirement would be minimized (Kaushik and Medale, 1994) and support a quick increase in the population biomass when environmental conditions improve in the spring. In addition, the over- wintering juvenile icefish have a longer growth period, which may itself occupy a position of prominence when competing for food with larvae of contemporaneous native fish species that also spawned in the spring.

Impacts of icefish introduction Our results showed obvious phenotypic plasticity and flexibil- Fig. 5. Percentage of gonad development in different stages for ity in life-history traits of icefish. This was typically shown in female icefish, Lake Erhai, June 2009 to December 2010. Sample successfully invasive fishes (Fox et al., 2007; Novomeska and sizes = 30 females each month Kovac, 2009), and highlights the ability of icefish to establish populations in different environments. In fact, icefish not rainy or dry season, and the water area and water level are only established a population in Lake Erhai, but also became relatively stable. The water temperature difference between a dominant species. As a zooplanktivorous fish, the icefish seasons (10.2–22.6°C; average 16.9°C) is also not as high as could affect zooplankton densities (Liu, 2001) as well as the in the lakes in the middle and lower reaches of the Yangtze zooplankton community structure (Zhang et al., 2005). In River (4.0–29.4°C; average 17.0°C) (Wang and Dou, 1998). Lake Erhai, the dominant position and pronounced seasonal In addition, the level of predation risk and food competi- fluctuation in the icefish population may promote this effect. tion was also lower than in the native and some other All native fishes in the lake forage on planktonic organisms introduced icefish areas (as already mentioned). This may during their early life-history stages, and some native fishes suggest that such a stable and unconstrained environment are even filter-feeders as adults (Xie and Chen, 2001), thus in Lake Erhai provided the icefish with an easy living. Also, the intensive feeding by the icefish can affect the food needs spawning once a year better fit the fluctuation of the water of the native fishes. This results in a significantly negative

Fig. 6. Monthly mean GSI ( 2 SE, all n = 30) of female iceﬁsh in relation to mid-water temperature, Lake Erhai, June 2009 to May 2010. Temperature curve = monthly means, smoothed over time 868 F.-Y. Zhu et al.

Table 3 VBGF parameters of iceﬁsh populations in diﬀerent areas of China

Latitude and L∞ 0 Location Longitude Status (mm)* kt0 φ Source

Lake Erhai, Yunnan Province N25°360–25°570 Introduced 96.1 1.61 0.26 4.17 Present study E100°060–100°170 Lake Wanghu, Hubei Province N29°500–29°540 Native 68.0 2.52 0.03 4.06 Yin et al., 1997 E115°170–115°230 Xinanjiang Reservoir, Zhejiang Province N29°240–29°450 Introduced 80.0 0.124 0.198 2.90 Xu and Luo, 1996 E118°400–119°120 Lake Dianchi, Yunnan Province N24°400–25°000 Introduced 67.0 0.198 0.225 2.95 Wang et al., 1998 E102°360–102°470 Lake Fuxian, Yunnan Province N24°210–24°370 Introduced 78.7 0.47 0.44 3.46 Qin et al., 2009 E102°490–102°570 Qingshitan Reservoir, Guangxi Province N25°280–25°320 Introduced 70.6 0.247 0.4145 3.09 Yang et al., 2001 E110°090–110°110 Miyun Reservoir, Beijing N40°180–40°200 Introduced 80.1 0.269 0.2486 3.24 Wang et al., 1990 E116°350–116°370 Xujiahe Reservoir, Hubei Province N31°390–31°300 Introduced 65.1 0.239 0.507 3.01 Wang et al., 1996 E113°340–113°430 Xinfengjiang Reservoir, Guangdong Province N23°420–23°580 Introduced 88.0 0.217 0.125 2.70 Xiao et al., 2002 E114°200–114°420

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