Environ Biol Fish (2013) 96:895–903 DOI 10.1007/s10641-012-0085-3
Reduced growth and reproductive investment of Hemiculter leucisculus (Cyprinidae) in a reservoir with introduced icefish Neosalanx taihuensis (Salangidae) Xinglu Wang & Jianguo Xiang & Jiashou Liu & Ming Liu & Lang Wu & Brian R. Murphy & Songguang Xie
Received: 10 January 2012 / Accepted: 20 September 2012 / Published online: 3 October 2012 # Springer Science+Business Media Dordrecht 2012
Abstract Neosalanx taihuensis is an important zooplanktivorous commercial fish that has been widely introduced into Chinese freshwaters. Introduction of this species has induced decline and even extinction of native fish species in some waters. In this study, impacts of N. taihuensis introduction on growth and reproductive characteristics of an indigenous zooplanktivorous fish Hemiculter leucisculus were investigated by comparing population traits of the latter species in two reservoirs X. Wang : J. Liu : M. Liu : L. Wu : S. Xie (*) The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Hubei, People’s Republic of China e-mail:
[email protected] X. Wang : L. Wu Graduate School of Chinese Academy of Sciences, Beijing 100039, People’s Republic of China
that differ only in whether N. taihuensis has been introduced. Huangshi Reservoir (HSR) and Mengquan Reservoir (MQR) are geographically proximate and display similar nutrient regimes and native fish faunas, but N. taihuensis has been stocked only in HSR. Populations of H. leucisculus in both reservoirs consisted of three age groups, ranging from age 1 to 3. Standard length (SL), body weight and backcalculated SL-at-age of H. leucisculus in HSR were significantly less than in MQR for both males and females in each age group. Female H. leucisculus also tended to produce fewer and smaller eggs (indicated by lower absolute fecundity, gonad weight and smaller egg diameter) in HSR than in MQR for each age group. We suggest that reduced growth and reproductive investment by H. leucisculus in HSR are likely the result of N. taihuensis introduction.
X. Wang : M. Liu : L. Wu : S. Xie Huai’an Research Center, Institute of Hydrobiology, Chinese Academy of Sciences, Huai’an, Jiangsu 223002, China
Keywords Neosalanx taihuensis . Invasive species . Hemiculter leucisculus . Planktivorous competition . Growth . Reproduction
J. Xiang School of Zoological Science and Technology, Hunan Agricultural University, Changsha 410128, Hunan, People’s Republic of China
Introduction
B. R. Murphy Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA
Biological invasion has been recognized as one of the major threats to biodiversity (Sala et al. 2000; Ruesink 2005; Vitule et al. 2009). Non-indigenous species (NIS) can impact ecosystems through competition with and predation on native species, thereby further
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threatening the structure and function of the receiving ecosystem (Mack et al. 2000; Carpenter et al. 2007). Declines and even extinctions of some native fish species have been attributed to species invasion (Dudgeon et al. 2006; Arismendi et al. 2009; Copp et al. 2009). An understanding of the interactions of NIS with native species is essential to an evaluation of the impacts of NIS on invaded ecosystems, and consequently for management and conservation. Neosalanx taihuensis (Wu 1931) is a freshwater icefish mainly inhabiting the middle and lower reaches of the Yangtze River, typically in its affiliated lakes (Chen 1956). Because of its high commercial value, N. taihuensis has been introduced into lakes and reservoirs in over 20 provinces, and has become the most commercially exploited icefish in China (Hu et al. 1998). N. taihuensis is a zooplanktivore, feeding primarily on Cladocera and Copepoda throughout its life and using mainly the middle and upper volume of the water column (Qin et al. 2007; Chen and Zhu 2008). This species’ life span is 1 year (Gong et al. 2009a). When successfully colonizing a new water body, its population typically blooms within several generations (Gong et al. 2009b), which can induce a zooplankton-resource shortage in the concerned waters (Guo and Xie 2005; Liu et al. 2009a, b). Icefish introductions have been observed to induce abundance decline and alteration of zooplankton species composition (Liu et al. 2009a, b). Similarly, N. taihuensis has been suggested to induce decline (and even extinction) of some native fishes due to food competition, especially fishes in the fragile subtropical lakes of Yunnan-Guizhou Plateau (e.g., Cyprinus megalophthalmus, Cyprinus longipectoralis and Anabarilius grahami) (Pan et al. 2007; Qin et al. 2007; Liu et al. 2009a, b). However, the mechanisms and processes underlying such impacts have never been investigated. We hypothesized that the introduction of N. taihuensis may stunt growth and reduce potential reproductive investment of native zooplantivorous species. Hemiculter leucisculus (Basilewsky 1855) is a smallsized planktivorous fish occupying a wide-range of Chinese rivers and lakes (Dai and Yang 2003). The age at first maturity is 1 year in most waters (Li et al. 2009), and it is not usually a commercially targeted fishery species. In this study, we tested this hypothesis by comparing growth and reproductive traits of H. leucisculus in two reservoirs, one with and one without introduced N. taihuensis.
Environ Biol Fish (2013) 96:895–903
Methods Study area Huangshi Reservoir (HSR; 29°11′–29°17′ N, 111°5′– 111°13′ E) is located upstream of Baiyang Stream, a tributary of the Yuan River which flows into Dongting Lake (Fig. 1). It was impounded in 1970 with an area of 4,380 ha and a catchment of 5.52×104 ha with a 95.0-m average water level. Mengquan Reservoir (MQR; 29°24′–29°26′ N, 111°21′–111°23′ E) is located upstream of Tao Stream, a tributary of the Li River which also flows into Dongting Lake (Fig. 1). It was impounded in 1981 with an area of 400 ha and a catchment of 6,960 ha with a 90.0-m average water level. The distance between the dams that form the two reservoirs is 26.9 km, so their climatological conditions are essentially identical. Both reservoirs are protected drinking-water sources. Seasonal waterquality variables including total phosphorus (TP, mgL−1), ammonia nitrogen (NH4–N, mgL−1), dissolved oxygen (DO, mgL−1), and BOD5 (mgL−1) were observed in both reservoirs by the Changde Environmental Protection Bureau in March, June, September and December both 2008 and 2009 and in March and June 2010 (http://slj.changde.gov.cn/art/ 2008/6/30/art_12291_100394.html). For the monitoring, water was sampled close to the dam. In each sample, water was sampled at three depths: 0.5 m below the surface, 0.5 m above the bottom sediment, and at 1/2 the depth of the water column; and then mixed. N. taihuensis was first introduced into HSR in 2000. Annual catch has been relatively stable at about 100 tons (http://www.cdcity.gov.cn/cdsslj/ 2308657758980800512/20050527/36682.html) for the last several years. Icefish were never introduced in MQR. There are no other commercial fish stocked in either reservoir. H. leucisculus is a very abundant fish in both reservoirs (unpublished materials). Fish sampling and processing H. leucisculus was sampled on 14 and 16 June 2009 at HSR using a lift net of 42×25 m (mesh size: 5 mm). Sampling occurred with a lift net of 30×30 m (mesh size: 5 mm) at MQR on 18 and 19 June 2009. Sampling was conducted in the evening. Each net was set with a 200-W light bulb approximately
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a Yangtze River
Li River
Dongting
29° 20’
Lake Yuan River 10 km 28° 40’ N 113° 00’ E
112° 00’
111° 00’
c
b
Tao Stream
1km
Baiyang
1km
S Fig. 1 Huangshi Reservoir (HSR, b) and Mengquan Reservoir (MQR, c) in the Dongting Lake watershed (a) in China. Black dots indicate the sampling locations for the present study; short bold lines mark the dams
2.5 m above the water surface to attract fish. Since H. leucisculus dies immediately upon capture, all specimens were placed directly on ice and later processed in the laboratory. Fish were aged using scales taken between the lateral line and the anterior of the dorsal fin on the left body side (Li et al. 2009). All the fish had new annulus formation evident in the scales. Each fish was assigned a calendar age equal to the number of annuli on the scale. Fish were then individually measured for standard length (SL, 0.1 mm) and weighed for body mass (BW, 0.01 g), and then condition factor (K; K0100×BW/SL3) was calculated for each fish.
Back-calculated SL-at-age was calculated using the direct proportion method by the measured annuli ratio and estimated age (DeVries and Frie 1996). The fish was then dissected and its sex was identified by inspecting the gonads. For females, the gonads were then removed and weighed (GW, 0.001 g). H. leucisculus is a single spawner with the oocytes developing synchronously (Sun et al. 2010). Females with gonads at stage IV and V (according to Li et al. 2008) were selected for fecundity determination. A subsample (ca. 0.05 g) of the ovary was removed, weighed (GWs, 0.001 g), and preserved in a 5 %
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neutral-buffered formalin solution. The number (n) of vitellogenic oocytes was counted under a dissecting microscope. Absolute fecundity (AF) was calculated as: AF ¼ n GW =GW s . Egg diameter was stochastically measured for over 30 vitellogenic oocytes from each subsample of stage-V gonads.
Table 1 Water-quality variables (mean ± SD with range beneath) in Huangshi Reservoir (HSR) and Mengquan Reservoir (MQR). Monitoring was conducted seasonally by the Bureau of Changde Environmental Protection in March, June, September and December both 2008 and 2009 and in March and June 2010 (http://www.cdhbj.gov.cn/col/col11436/index.html). The results of pairwise t-tests for difference of these variables between the two reservoirs are presented
Statistical analysis
Water chemical index
Seasonal water-quality variables were compared between HSR and MQR using a pairwise t-test. ANOVA was applied for SL, BW, K and the back-calculated SL-at-age with age, population (HSR and MQR) and sex as independent variables, and for AF of females with age and population as independent variables. Differences in GW and AF of females between the two populations were also tested using ANCOVA with BW as a covariate. Nested ANOVA was applied for egg diameter with age and population as independent variables and individual as a random variable nested in population. When the effect was significant, a multiple comparison of unequal HSD was applied to compare the difference between means. SL, BW and AF were loge-transformed to homogenize the variances of the variables. The data were expressed as mean ± SD and analyzed statistically at the p< 0.05 level. The analyses were conducted using STATISTICA 6.0 (StatSoft 2001).
Results The averages of TP, NH4–N, DO, and BOD5 were not significantly different between the two waters (Table 1). Both males and females were composed of three age groups (age 1, 2 and 3) in HSR and MQR. Population, sex and age had significant effects on SL and BW (Table 2). SL and BW increased significantly with age for each sex in each population. Age-1 males and females were not significantly different in SL and BW in MQR; while females were significantly larger in SL and BW than males for each age group in HSR and at age 2 and age 3 in MQR. H. leucisculus from HSR was significantly smaller in SL and BW than from MQR for each sex at each age. Mean SL of females from HSR was about 20 mm smaller than from MQR for each of the three age groups; BW of females from HSR was 64 % at age 1, 42 % at age 2 and 51 % at age 3 of the BW of similar-aged females
HSR
MQR
Pairwise t-test d.f. t
p
DO (mgL−1)
8.6±1.9 5.2–11.1
9
−1.739 0.116
TP (mgL−1)
0.03±0.01 0.02±0.02 9 0.01–0.06 0.01–0.07
−1.350 0.210
NH4-N (mgL−1) 0.21±0.15 0.20±0.20 9 0.05–0.47 0.05–0.86
−0.052 0.960
BOD5 (mgL−1)
−1.795 0.106
1.6±1.5 0.1–5.7
7.8±1.5 5.8–10.3
0.8±0.6 0.1–1.8
9
from MQR (Table 2). K was significantly affected by sex, being higher for females than for males, but not by population and age for the two reservoirs (Table 2). Sex, age and population affected the back-calculated SL of H. leucisculus significantly (Fig. 2; ANOVA, p< 0.05). Back-calculated SL of H. leucisculus was significantly larger in HSR than in MQR at each age for both females and males. Meanwhile, back-calculated SL increased significantly with age for both females and males in both populations, and back-calculated SL of females was significantly larger than males at age 2 and age 3 in both populations (Fig. 2; p
