Phenotypic Shifts in Life History Traits Influence Invasion Success of Goldfish in the Yarlung Tsangpo River, Tibet

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1 Transactions of the American Fisheries Society 144: , 2015 Ó American Fisheries Society 2015 ISSN: print / online DOI: / ARTICLE Phenotypic Shifts in Life History Traits Influence Invasion Success of Goldfish in the Yarlung Tsangpo River, Tibet Chunlong Liu Laboratory of Biological Invasion and Adaptive Evolution, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan , China; and Graduate University of the Chinese Academy of Sciences, Beijing , China Yifeng Chen* Laboratory of Biological Invasion and Adaptive Evolution, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan , China Julian D. Olden School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98105, USA Dekui He, Xiaoyun Sui, and Chengzhi Ding Laboratory of Biological Invasion and Adaptive Evolution, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan , China Abstract Goldfish Carassius auratus have been established in myriad ecosystems outside of their native ranges, and part of their successful establishment in new ecosystems might be attributed to the shift in life history traits. To explore the role of phenotypic shifts in Goldfish invasions, we quantified and compared spawning times and growth rates in the early life history of nonnative Goldfish from Chabalang and Chongdui wetlands in the Yarlung Tsangpo River basin. Spawning of nonnative Goldfish began on March 20 and April 14 for the Chabalang and the Chongdui populations, respectively, and both were considerably earlier than native populations despite the cold environments in the Yarlung Tsangpo River basin. Growth rates for the Chabalang population were significantly higher than those for the Chongdui population during the first 14 d posthatch; however, growth rates for the Chongdui population became higher after the 37th day. Within the Chabalang population, Goldfish hatching later had faster growth rates than individuals hatching earlier. Consequently, it seems that shifts in the timing of spawning and growth rates play an important role in the invasion success of Goldfish in extremely cold climates. Studying patterns of biological diversity has been the foundation of numerous ecological pursuits over the past two centuries. Recent decades have witnessed significant reshuffling of freshwater fish faunas caused by numerous intentional and unintentional introductions of nonnative species (Marr et al. 2010; Olden et al. 2010; Cucherousset and Olden 2011; Correa and Hendry 2012). Biological invasions consist of three sequential phases: the introduction of propagules into a new ecosystem, the establishment of self-sustaining population, and the assimilation of the nonnative species into the recipient ecosystem (Garcıa-Berthou et al. 2005; Feiner et al. 2012). Identifying the primary mechanisms by which nonnative species progress through each phase of the invasion process is essential for guiding management strategies aimed at prevention, control, and eradication of nonnative species (Lodge et al. 2006). 602 *Corresponding author: chenyf@ihb.ac.cn Received January 9, 2014; accepted December 1, 2014

2 PHENOTYPIC SHIFTS INFLUENCE GOLDFISH INVASION 603 Phenotypic shifts play an important role in the successful transition through different phases of the invasion process (Quinn et al. 2001; Sexton et al. 2002; Feiner et al. 2012). In general, phenotypic shifts of nonnative species are supported by two major mechanisms: phenotypic plasticity and genetic adaptation (Quinn et al. 2001; Sexton et al. 2002; Richards et al. 2006). For example, high phenotypic plasticity in life history traits allow invaders to withstand a wide range of environmental conditions, thus facilitating their rapid establishment in new ecosystems (Sexton et al. 2002; Richards et al. 2006). Once established, genetic adaptation (e.g., evolution and recombination) allows nonnative species to withstand novel selection pressures (Haugen and Vøllestad 2001; Sexton et al. 2002). By means of rapid adaptive evolution and genetic recombination, nonnative species could evolve the optimum phenotype under a stable environment and increase individual fitness consequentially (Hendry and Kinnison 1999; Aday et al. 2003; Hendry et al. 2008; Meril a and Hendry 2014). Systematic studies evaluating the role of phenotypic shifts in the invasion success of nonnative fishes are relatively limited. We aimed to address this knowledge gap by studying introduced populations of Goldfish Carassius auratus in the Yarlung Tsangpo River basin, China, to elucidate the importance of shifts in life history traits for shaping their establishment success. The Yarlung Tsangpo River is the largest river on the Qinghai Tibet Plateau and exhibits mean monthly water temperature ranging from 1 Cto15 C (Tang and Xiong 1998; Huang et al. 2011). Water temperature is a fundamental ecological resource (Magnuson et al. 1979) that can affect all phases of the invasion process (Rahel and Olden 2008). Warming temperatures have been linked to range expansions of nonnative species and heightening of their impacts on native species (e.g., Taniguchi et al. 1998; Cucherousset and Olden 2011). Similarly, minimum water temperature and the extent of ice cover on streams and lakes may influence the invasion process by changing oxygen conditions (Rahel and Olden 2008). However, several nonnative fishes have established populations in the Yarlung Tsangpo River in recent years despite its cold thermal conditions (He et al. 2013; Huo et al. 2013). Among these species is the Goldfish, which displays an establishment rate exceeding 92% in its introduced range and is the highest among the 10 most frequently introduced aquatic species globally (Garcıa-Berthou et al. 2005; Lorenzoni et al. 2010). Our study examines the question of whether rapid phenotypic shifts have afforded Goldfish the opportunity to establish self-sustained populations in the cold thermal conditions of the Yarlung Tsangpo River basin. We predicted that introduced Goldfish had evolved an earlier spawning time to extend the length of the first growing season. Furthermore, to maximize survival, we expected that Goldfish from different populations would exhibit distinct growth patterns in response to environmental conditions. To test these hypotheses, we surveyed Goldfish over the whole year in the Yarlung Tsangpo River basin and quantified the spawning time and growth rates in early life history using otolith microstructure analysis. METHODS Study area and sampling. The study area in the Yarlung Tsangpo River basin included two wetlands chosen for their differences in geology and hydrology (Figure 1). The Chabalang wetland ( E, N; 3,569 m) is located in the Lhasa River, which is the largest tributary of the Yarlung Tsangpo River and exhibits a mean monthly water temperature ranging from 0.8 C to 13.9 C (Tang and Xiong 1998). The Chongdui wetland ( E, N; 3,900 m) is located in the mainstream of the Yarlung Tsangpo River and exhibits a mean monthly water temperature ranging from 0.9 C to 15.4 C (Tang and Xiong 1998). Fish surveys were conducted monthly for the period from May 2004 to March 2005 at the Chabalang wetland (except August 2004 and February 2005) and twice in April 2005 at the Chongdui wetland. We conducted standardized sampling using a gill net (20 1 m; 1-cm mesh size). One gill net was deployed across the nearshore transect of the wetland at 2000 hours and retrieved at 0600 hours the following day. All Goldfish were measured to the nearest 0.1 mm and weighed to the nearest 0.1 g, then preserved in a 70% solution of ethanol. Early life histories of Goldfish were studied in the Chabalang wetland during May 2011 and in the Chongdui wetland during July Young of year (age-0) Goldfish were collected by dipnetting (50-cm diameter with 0.5-mm mesh size) and electrofishing schools of Goldfish during the daytime. Sampling effort was standardized (20 min/sampling event) and relative abundances of age-0 Goldfish at the two wetlands were determined by CPUE (the average number of Goldfish captured in one dip net). All samples were preserved in a 70% ethanol immediately after sampling and then taken back to the laboratory. In the laboratory, the standard length (SL) of each individual was measured to the nearest 0.1 mm. The possible shrinkage in length caused by ethanol preservation was ignored. We used a standard described by Chen (1959) and Cao et al. (2007) to categorize the developmental stage in the early life history of Goldfish: larvae (<7.4 mm SL) or juveniles ( mm SL). Fish culture experiment. Fish cultured experiments were conducted for validating the daily periodicity of otolith deposition. Adult female and male Goldfish were bought from State Key Laboratory of Freshwater Ecology and Biotechnology (Chinese Academy of Sciences, Wuhan, China). In May 2012, eggs were artificially fertilized in the laboratory and then incubated at 25 C under 24-h light. After hatch, 100 larvae were moved into a 15-L tank held at 15 C and a light cycle of 12 h light : 12 h dark. Five to eight larvae were sampled daily over

3 604 LIU ET AL. FIGURE 1. The Yarlung Tsangpo River, including the two sampling sites of nonnative Goldfish: Chabalang wetland, indicated by the circle, and Chongdui wetland, indicated by the square. Inset depicts the introduced (I) and native ranges (N) of Goldfish in China. a 14-d posthatch period and preserved at 20 C in a 5-mL centrifuge tube for subsequent otolith analysis. Otolith preparation and measurement. Right and left otoliths were extracted from both wild and cultured Goldfish under a dissecting microscope. Otoliths of cultured Goldfish were small and could be interpreted readily without any further processing. We cleaned those otoliths and covered them on glass slides with nail polish. Otoliths of wild Goldfish were relatively larger. The right otolith of each larva was mounted on the glass slide with thermoplastic glue and then polished using 15-mm lapping film until the nucleus and all increments became well defined. Each otolith section was photographed at 400 magnification using the digital camera fixed on a light microscope (BH2; Olympus Optical, Tokyo, Japan). Otolith increment numbers and widths were counted and measured along the maximum otolith radius (OR) from the nucleus to the edge using Increment Analysis Program (Huazhong Agricultural University, Wuhan, Hubei Province, China; Figure 2). Two independent evaluations for each otolith were made. If the two evaluations differed by <5%, one count was selected as the otolith increment number randomly; otherwise the otolith section was measured again. If the third evaluation differed by <5% in comparison to either of the first two evaluations, then the third evaluation was used as the otolith increment number. If the third evaluation still differed the first two evaluations by >5%, that otolith section was discarded. Of the measured 410 otolith sections, 359 were used for otolith microstructure analysis; this included 279 otolith sections of wild Goldfish (183 for the Chabalang population and 96 for the Chongdui population) and 82 otolith sections of cultured Goldfish. Data analysis. Linear regression analysis was used to assess the relationship between fish age (d) and otolith FIGURE 2. An otolith section of a 24-d-old Goldfish from the Chabalang wetland. The nucleus (N) and the maximum otolith radius (OR) are indicated by arrows. Increment numbers and widths were counted and measured along the OR. [Figure available online in color.]

4 PHENOTYPIC SHIFTS INFLUENCE GOLDFISH INVASION 605 increment number for the cultured Goldfish. Slope of the linear regression was compared to 1 using ANCOVA. Otolith increment numbers of right and left otoliths were compared using paired t-test. Relationships between SL and OR of wild Goldfish for the Chabalang population and the Chongdui population were fitted by linear regression separately. Daily somatic growth rates were back-calculated using the biological intercept method, where the biological intercept of Goldfish was the SL at hatching (Campana 1990). Ages (d) of wild Goldfish were estimated as the number of otolith increments minus the number of increments deposited before hatch. Hatch dates were back-calculated by subtracting ages from catching dates (May 27 for the Chabalang population and July 9 for the Chongdui population). Because the incubation period of Goldfish eggs typically exceed 15 d at a water temperature <10 C (Yin 1995), spawning dates of age- 0 Goldfish were deduced by subtracting the conservative 15 d from hatch dates since water temperature in the Yarlung Tsangpo River was <10 C before the hatching periods (Tang and Xiong 1998). Fish hatching on different dates encountered distinct environments within the same population (Bacha and Amara 2012). To explore the influence of changing environmental factors on fish growth, Goldfish from the Chabalang wetland were divided into three groups according to hatch date. Early groups were defined as Goldfish hatching from April 5 to April 19, middle groups were hatching from April 20 to May 1, and late groups were hatching from May 2 to May 13. Daily growth rates among three groups were compared using repeated-measures ANOVA (RM-ANOVA; Searcy and Sponaugle 2000). Because the minimal fish age of wild Goldfish was 14 d among the two populations (see Results), the level of RM-ANOVA was set as 14 for covering all individuals. Daily growth rates during the first 14 d were defined as the withinsubject factor, and three groups were defined as the betweensubject factor. Similarly, growth rates of wild Goldfish from the two wetlands were compared using RM-ANOVA. Lastly, we compared spawning onsets of introduced Goldfish with those of Goldfish in native and other introduced ranges (Chen 1959; Huang et al. 1980; Li et al. 2006; Lorenzoni et al. 2010) and those of three native fishes in the Yarlung Tsangpo River basin (Jia and Chen 2009; Qiu and Chen 2009; X. Li, Y. Chen, and D. He, paper presented at a Chinese Ichthyological Society symposium, 2008) to test for potential changes in Goldfish spawning time in the Yarlung Tsangpo River basin. RESULTS Population Status A total of 453 Goldfish were collected at the Chabalang wetland during the year-long survey; the fish ranged in size from 24.5 to mm SL and in weight from 0.4 to g (Table 1). In April 2005, we collected 36 Goldfish at Chongdui wetland ranging from 62.1 to mm and from 8.6 to 47.8 g in SL and weight, respectively (Table 1). At the Chabalang wetland, Goldfish could be sampled every month, indicating that they had survived the whole year in the Yarlung Tsangpo River basin. In 2011, a total of 212 age-0 Goldfish were collected at the Chabalang wetland, with SL ranging from 8.3 to 25.1 mm. In the Chongdui wetland, 106 Goldfish were collected, with SL ranging from 14.7 to 49.5 mm (Table 1). The proportions of Goldfish whose SL exceeded 16.0 mm were 30.2% and 63.5% for the Chabalang population and the Chongdui population, respectively, indicating that wild Goldfish survived through the early life history (larval and juvenile stages). Based on the above findings that Goldfish survived the whole year and early life history successfully, nonnative Goldfish have established self-sustained populations successfully in the Yarlung Tsangpo River basin. TABLE 1. Summary statistics for nonnative Goldfish captured from Chabalang and Chongdui wetlands in 2004, 2005, and Wetland Sampling date Number of specimens Length (mm) Weight (g) Maximum Minimum Maximum Minimum Sampling instrument Chabalang May Gill net Jun Gill net Jul Gill net Sep Gill net Oct Gill net Nov Gill net Dec Gill net Jan Gill net Mar Gill net May Dip net, electrofishing Chongdui Apr Gill net Jul Dip net, electrofishing

5 606 LIU ET AL. FIGURE 3. Relationships between standard length and otolith radius of Goldfish from the Chabalang and Chongdui wetlands in Otolith Deposition Validation The SL (mean SD) of newly hatched Goldfish was mm. Otolith increment number (I N ) and age (D [d]) of cultured Goldfish were positively correlated (I N D 1.03D C [R 2 D 0.98, P < 0.01]). This suggests that one otolith increment was deposited at hatch, and one increment was deposited daily after hatch. No significant difference was found in increment numbers between right and left otoliths (P > 0.05), indicating that either otoliths are suitable for otolith microstructure analysis. Life History Traits We found strong positive relationships between SL and OR of wild Goldfish for the Chabalang population (OR D 14.5 SL 23.3, R 2 D , P < 0.01) and the Chongdui population (OR D 16.3 SL 60.9, R 2 D , P < 0.01; Figure 3). The Chabalang population exhibited a considerably earlier spawning period (March 20 April 28) and earlier hatching period (April 5 May 13) than the Chongdui population (April 14 May 22 and April 29 June 8, respectively; Figure 4). Growth rates for the Chabalang population were significantly higher than those for the Chongdui population during the first 14 d posthatch (P < 0.01; Figure 5); however, growth rates for the Chongdui population became higher after the 37th day. At the end of the observational period, SLs for the Chabalang and Chongdui populations averaged 19.7 and 18.4 mm, respectively. This suggests that Goldfish from the two wetlands achieved similar final SLs despite substantial differences in initial growth rates. In the Chabalang wetland, we found significant differences in growth patterns of Goldfish for the three groups displaying different dates for the onset of hatching (F D 15.4, df D 13, P < 0.01; Figure 6). The early hatching group exhibited the FIGURE 4. Hatch dates back-calculated from otolith increment numbers of age-0 Goldfish from the Chabalang and Chongdui wetlands in FIGURE 5. Growth trajectories of Goldfish from the Chabalang and Chongdui wetlands in Days on which less than five Goldfish were captured were excluded. Confidence intervals of growth rates are represented by error bars.

6 PHENOTYPIC SHIFTS INFLUENCE GOLDFISH INVASION 607 FIGURE 6. Posthatch growth trajectories of Goldfish from the Chabalang wetland in Fish were divided into three groups according to their spawning period (see Methods). Confidence intervals of growth rates are represented by error bars. slowest growth rate, ranging from 0.13 to 0.17 mm/d (P < 0.01), and the late-hatching group exhibiting the fastest growth rates, ranging from 0.20 to 0.39 mm/d (P < 0.01). This suggests that the shorter growing seasons (from May) for the late group may ultimately be offset by higher daily growth rates. There were significant differences in spawning onsets of Goldfish between native and introduced ranges (Table 2). Goldfish began spawning from May and June in native ranges but from March or April in the Yarlung Tsangpo River basin and Lake Trasimeno, indicating Goldfish advanced spawning time after being introduced into new ecosystems. Additionally, in our study, spawning onsets of nonnative Goldfish were similar to those of indigenous fishes in the Yarlung Tsangpo River basin, including Oxygymnocypris stewartii, Ptychobarbus dipogon, and Schizothorax waltoni, which begin spawning from March, April, and April, respectively (Table 2). DISCUSSION Our study suggests divergent strategies for nonnative Goldfish in the Yarlung Tsangpo River basin to cope with the cold environments. Goldfish exhibit significant shifts in life history traits, as evidenced by the fact that they spawn earlier than Goldfish in native ranges and adopt distinct growth patterns under different environments. In native ranges, spawning of Goldfish is induced by a water temperature exceeding 15 C (Chen 1959). However, Lorenzoni et al. (2010) reported that spawning of nonnative Goldfish in Lake Trasimeno occurred at a water temperature of 13 C, indirectly suggesting that high water temperature was not the prerequisite for Goldfish spawning in introduced ranges. Our results further indicate that nonnative Goldfish could spawn and persist in extremely cold environments because mean monthly water temperature in the Yarlung Tsangpo River basin is only between 4 C and 8 C during their spawning seasons (March and April; Tang and Xiong 1998). Spawning time is one important trait affecting invasion success, which controls fish survival and drives the strength of year-classes (Quinn et al. 2002; Bacheler et al. 2008). By spawning earlier, nonnative Goldfish may extend their first growing season (from April) and possess advantages in sizes for reducing vulnerability and accelerating their establishment in new ecosystems. Environmental and biological differences between the two wetlands are likely driving differences in growth rates between the Goldfish populations. Growth rates often correlate strongly with resource availability (Bacha and Amara 2012; Garcıa- Berthou et al. 2012); therefore, the observed lower growth rates in the Chongdui wetland is likely because it is the least productive wetland in the Yarlung Tsangpo River basin (Rao 1964). In addition, population density has direct impacts on growth rates (Lorenzen and Enberg 2002; Feiner et al. 2012). Population density of age-0 Goldfish at the Chabalang wetland was approximately three times higher than that of the Chongdui population (C. Liu, unpublished data). In summary, reduced Goldfish growth rates in the Chabalang wetland is likely the result of more intense intraspecific competition and reduced food availability to support development during the late ontogeny. We found that nonnative Goldfish at Chabalang wetland exhibited variable hatching times that translated into distinct growth patterns during their early life history. Specifically, Goldfish hatching later had faster growth rates than individuals hatching earlier. Increasing water temperature with time is the likely mechanism because Goldfish growth rates are positively correlated with temperature up to 28 C (Kestemont 1995). TABLE 2. Comparison of spawn timing of Goldfish from introduced and native (China) populations. Status Location Spawning onset Elevation (m) Longitude (E) Latitude (N) Source Introduced Chabalang wetland Mar 3, Present study Introduced Chongdui wetland Apr 3, Present study Introduced Lake Trasimeno Mar Lorenzoni et al. (2010) Native Liangzi Lake May Chen (1959) Native Nanwan Lake Jun Li et al. (2006) Native Baiyangdian Lake May Huang et al. (1980)

7 608 LIU ET AL. During the growing season (from April) of age-0 Goldfish, water temperature in the Yarlung Tsangpo River rises rapidly from 4 Cto10 C (Tang and Xiong 1998), thus improving individual feeding and metabolic rates, and also increasing food availability (Cross et al. 2009; Bacha and Amara 2012). Taken together, we suspect that substantial trade-offs exist between spawning times and growth rates (Heino and Kaitala 1999; Zera and Harshman 2001). Late-spawning Goldfish may compensate for a shorter growing season (from May) by exhibiting more rapid growth rates; ultimately, these fish may achieve similar sizes by the end of the first growing season compared with age-0 Goldfish produced by earlier spawning fish. It is important to note that our study precludes the ability to disentangle the relative contributions of phenotypic plasticity and genetic adaptation to shifts in Goldfish spawn timing and growth rates. Previous studies have demonstrated that phenotypic plasticity allows nonnative species to express advantageous phenotypic traits in the initial invasion stage to accelerate their establishment (Sexton et al. 2002; Richards et al. 2006), and adaptive evolution would provide organisms different phenotypes later under new selective regimes to increase fitness (Sexton et al. 2002). However, the interplay of phenotypic plasticity and genetic adaptation vary during invasion (Quinn et al. 2001). In the future, additional research is needed to better understand the relative contributions of phenotypic plasticity and genetic adaptation in shaping shifts in phenotypic traits. Predicting the potential spread of invasive species remains a core goal in conservation biology (Vander Zanden and Olden 2008), and life history traits continue to show utility in this regard (Feiner et al. 2012; Coulter et al. 2013). Our study suggests that shifts in the timing of spawning and growth rates play an important role in the invasion success of Goldfish in extreme cold climates. Future studies should consider how phenotypic shifts of introduced fishes is influencing the invasion process, and how this knowledge can be used to better manage invasive populations. ACKNOWLEDGMENTS This research was supported by the Natural Science Foundation of China (grant ) and National Basic Research Program of China (973 Program, grant 2009CB119200). We would like to thank Nathan M. Bacheler, Richard T. Eades, and two anonymous reviewers for their constructive suggestions on the manuscript; Juan Lei, Juan Tao, Weixing Tang, and Xiao Zhang for their help during sampling; and Junyan Jin for help in supplying the Goldfish. REFERENCES Aday, D. D., D. H. Wahl, and D. P. Philipp Assessing population-specific and environmental influences on Bluegill life histories: a common garden approach. Ecology 84: Bacha, M., and R. 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