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Maximum handling size, prey size and type selection


Aquaculture Research, 2014, 45, 720–727

doi:10.1111/are.12014

Maximum handling size, prey size and type selection by snakehead (Channa argus) feeding on juvenile Chinese mitten crab (Eriocheir sinensis)
Mingzhong Luo1,2, Tanglin Zhang1, Zhongjie Li1 & Jiashou Liu1
1

State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Graduate School of the Chinese Academy of Sciences, Beijing 100039, China

Sciences, Wuhan 430072, China
2

Correspondence: T L Zhang, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China. E-mail: tlzhang@ihb.ac.cn

Abstract
Laboratory predation trials were conducted to investigate maximum handling size, prey size and type selection by small (35–37 cm in total length, LT), medium (43–46 cm LT) and larger (58–60 cm LT) snakehead (Channa argus) when feeding on a wide size (9–34 mm in carapace width, CW) range of juvenile Chinese mitten crab (Eriocheir sinensis). The maximum handling size of predator feeding on crabs monotonically increased with predator LT and mouth gape width, GW. Snakehead with at least 16.0 cm LT or 27.7 mm GW would be capability to consume the smallest size group of crabs, whereas the predator with 72.6 cm LT or 63.4 mm GW would be capability to consume all size groups of crabs in these trails. Prey-size selection trials showed that snakehead has a high preference to the small-sized crabs, and lower preference to the medium or large size crabs. The preference index was signi?cantly affected by prey size and prey size 9 predator size interaction, however, was not affected by predator size. In prey type experiments, snakehead consumed lower proportions of juvenile crabs when fed on the crab and crucian carp than when fed on only the crab, which suggests alternative ?sh prey may reduce predation risk of the crab by snakehead in nature. These results could be useful for improving the ?shery management and release strategies for the crab.

Introduction Crustaceans, which include crabs, cray?sh and some aquatic insects often play important roles as prey for some species of piscivorous in fresh water system and marine (Young, Buzas & Young 1976; Stoner 1982; Dean & Connell 1987; Holmlund, Peterson & Hay 1990). Perch Perca ?uviatilis L. and eels Anguilla anguilla L. are considered to be two of the principal predators of cray?sh in Europe (Hamrin 1987; Blake & Hart 1995). Scharf and Schlicht (2000) suggested that blue crab Callinectes sapidus is an important component of red drum diets during spring and fall in Galveston Bay. Mortality induced by predation may limit prey recruitment processes in some aquatic ecosystems (Bailey & Houde 1989; Hartman & Margraf 1993; Bailey 1994). Speci?cally, predation occurs during early life stage of crustaceans, which have high vulnerability and lack of avoidance abilities (Gaines & Roughgarden 1987; Menge & Sutherland 1987; Smith & Herrnkind 1992; Eggleston & Armstrong 1995; Gosselin & Qian 1996). Then, early juvenile stage is thought to be critical period in the life cycle of crabs and causing a bottleneck in the recruitment (Moksnes, Pihl & Montfrans 1998). Many previous studies about predation on crabs focused on period of larvae, which carapace width (CW) less than 1 mm. However, juvenile crab of CW more than 10 mm, which always releasing in lake and ponds, are extraordinary signi?cant for crabs stock enhancement and culturing. Unfortunately, there is little information available concerning this aspect (see Moksnes et al. 1998).

Keywords: maximum handling size, prey selection, snakehead, Chinese mitten crab, feeding

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Aquaculture Research, 2014, 45, 720–727

Predation of snakehead on juvenile Chinese mitten crab M Luo et al.

The maximum handling-size of prey that a predator can feed on is constrained by predator’s morphological constraints, speci?cally the size of feeding apparatus (e.g. mouth gape) (Werner 1974; Persson, Anderson, Wahlstrom & Eklov 1996; Brooking, Rudstam, Olson & Vandevalk 1998; Nilsson & Bro ¨ nmark 2000; Do ¨ rner & Wagner 2003; Holly & Thomas 2005) and differences in spatial scales in combination with the swimming abilities of predator and prey (Christensen 1996). Claessen, Oss, Roos and Persson (2002) suggested that the maximum handling size mainly affects prey and predator’s community structure and individual life history. Knowledge of the maximum handling size of crab captured by piscivorous ?sh would be useful for predicting the minimum releasing sizes of crab that would be safe in a given lake. Prey size and type selection is a major aspect within study of predatory ?sh feeding on crabs, may cause the direct in?uences on crab’s growth, survival, abundance, distribution and even antipredator behavioural changes (Moksnes et al. 1998; Jin, Li & Xie 2000; Scharf & Schlicht 2000). Chinese mitten crab is widely distributed in freshwater system and propagation in coastal and estuarine water, which is famous for its delicious taste and favoured in Chinese and Southeast Asia markets. The stock enhancement in lakes and ponds culturing of Chinese mitten crab are two main ?shery modes with high commercial bene?ts in Changjiang River areas. Snakehead Channa argus is one of the most typical piscivorous ?sh existed commonly with Chinese mitten crab in rivers and lakes. The aims of this study were to investigate: (1) maximum handling size of juvenile Chinese mitten crab that could be consumed by a rang sizes of snakehead, (2) prey size selection by small (35–37 cm total length, LT), medium (43–46 cm LT) and larger (58–60 cm LT) snakehead feeding on a three sizes of juvenile Chinese mitten crab and (3) prey type selection by medium-sized snakehead feeding on crabs (15–18 mm CW) and frozen crucian carp Carassius auratus simultaneously. Materials and methods Experimental animals Snakehead served as predators was caught in Taojia Lake, Hubei Province, China, and transported

to the laboratory in June 2008. The size range of snakehead was determined for this study, which was similar to the size range of individual commonly captured by ?shermen in ?ve typical lakes belong to the middle area of the Changjiang River (Ma, Xie & Gong 1997; Tan 1997; Xie, Xia, Zhu & Jin 1997; Zhang, Gong, Liu, He & Gao 1999; Yu, OuYang, Wu, Dai & Zou 2008). The predators were acclimatized to experimental conditions for a minimum of 3 weeks and maintained on a diet of frozen crucian carp (Carassius auratus) and live crab for a minimum of 2 weeks prior to the experiments, and all predators were trained to recognize prey through constant exposure during rearing. Juvenile Chinese mitten crabs as prey in the experiments, were collected from a ?shery in the vicinity of Wuhan City, Hubei Province, China, during summer and transported to the laboratory. Crabs were held in a 27 m3 concrete pool (9 9 3 9 1 m) with a water depth of 30 cm, and were fed commercial crab feed daily. These crabs ranged 9–34 mm in CW, which were similar to the size ranges of juvenile crabs commonly released in lakes along the middle reach of the Changjiang River for a commercial stocking ?shery. The trials were conducted in twenty 2400-L concrete pools with a water depth of 60 cm. The experiments were also carried out in a greenhouse, kept under a constant light regime (14 h light: l0 h dark) and temperature (23–27°C). The water was aerated and changed on a regular basis (>30% volume per week). Otherwise, the pools were kept bare to make all ?sh visible on crabs and to be able to evaluate the effects of feeding only, without other confounding factors. Each snakehead was starved for 24 h to standardize hunger levels prior to the experiments. Predators were mildly anesthetized with 100 mg L?1eugenol for measurement of LT, W and gape width (GW). The GW was measured (nearest mm) using a vernier caliper according to Do ¨ rner and Wagner (2003). The measured predators were put into the experimental pools randomly and one ?sh existed in each pool. To minimize manipulating stress, the predator in each pool was not to alter until it had experienced all feeding experiments. To avoid the effects of potential learning behaviour by crabs resulting from continuous holding in the experimental pools for extended periods, the survived crabs were removed and not used in other trials (Scharf et al., 1998).

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Aquaculture Research, 2014, 45, 720–727

Experimental design
Crab caracape width (mm)

30

(a)
28 26 24 22 20 18 16 14 30 35 40 45 50 55 60 65

Maximum handling size Maximum handling size of 19 snakehead ranging from 351 to 603 mm LT fed on crabs was determined using a series of feeding experiments. Each trial consisted of a single snakehead presented with ?ve crabs ranging from 9 to 34 mm CW (differences exceeding 1 mm between any two crabs in every trial) and allowed to feed for 48 h. Maximum handing size of predators were determined by retrieving and measuring uneaten crabs. Prey-size selection

Total length of snakehead (cm)
30

The trials were conducted by three size-classes of prey (CW): small (14.1–15.9 mm), medium (18.0– 19.9 mm) and large (22.1–23.9 mm) and three size-classes of predators (Table 1). Each feeding trial was performed with a single snakehead as predator and a total of 15 crabs (small, medium and large size, ?ve crabs of each size category) as prey. Prey crabs were exposed to the predator for 24 h; uneaten crabs were removed from pools, measured individually and weighed as a group, for the sake of identify sizes and weight, which had been consumed by snakehead. A total of 15 different predators (?ve ?sh from each size category) were used in feeding trials coinstantaneous, and then this pattern continued to repeat seven times for each predator (n = 105). Prey type selection In this experiment, prey type selection of snakehead was examined by presenting individual medium-sized ?sh (43–46 cm LT, 1015 ± 78.04 g) with crabs (15–18 mm CW, 2.14 ± 0.17 g) and frozen crucian carp simultaneously. A preliminary trial was conducted to measure the maximum weight of frozen crucian carp that single predator would consume daily. To investigate the effect of crucian carp on snakehead consuming crabs, approximately half of maximum weight and nearly maximum weight of frozen crucian carp were offered to each predator separately (Table 2). After 24 h, all uneaten prey (including crabs and crucian carp) were collected and measured individually. A total of 63 prey-type selection trials and 21 replicate trials in each of three treatments (high, low and 0 weight level of crucian carp) were conducted on consecutive 7 days.

(b)
28

Crab caracape width (mm)

26 24 22 20 18 16 14 35 40 45 50 55 60

Gape width of snakehead (mm)

Figure 1 The relationships between (a) total length (LT) and (b) mouth gape width (GW) of snakehead (predator) and maximum handling size in carapace width (CW) of Chinese mitten crab (prey).

Table 1 Predator and prey size category, morphometrics of the three predator size groups and carapace width of prey used in prey-size selection trials
Predator Size category
Small Medium Large

Prey W(g)
363–450 927–1170 2046–2212

LT (mm)
351–373 433–458 582–603

GW (mm)
38.2–40.1 44.0–48.9 51.1–55.8

CW (mm)
14.1–15.9 18.0–19.9 22.1–23.9

Data analysis Line regressions were used to analyze for relationships between LT of snakehead and maximum handling size of crab (CW), between GW of snakehead and maximum handling size of crab (CW) besides. Prey-size selectivity of each of three size

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? 2012 John Wiley & Sons Ltd, Aquaculture Research, 45, 720–727

Aquaculture Research, 2014, 45, 720–727

Predation of snakehead on juvenile Chinese mitten crab M Luo et al.

Table 2 Prey type and weight or number used in prey species selection trials
Common carp weight (g) in one trial
50 20 0

Common carp weight level
High Low 0

Crabs weight (g) (number) in one trial
21.5 ± 1.77 (10) 22.3 ± 1.31 (10) 20.2 ± 0.88 (10)

classes of predator for each of three sizes of prey was mathematical measured using Chesson’s preference index (PI) (Chesson, 1983), and is de?ned as: m X ai ? ?ri =pi ?= rj =pj ; i ? 1; :::; m
j?1

LT and GW. The slopes of the regressions were not signi?cantly different (ANCOVA, F1,36 = 0.0237, P > 0.05); however, elevation of GW was a little higher than LT. All ?sh in these feeding trials indicated ability to consume crabs, which smaller than 16 mm in carapace width, however, calculated using linear regression equations (Fig. 1), ?sh which at least 16.0 cm LT or 27.7 mm GW would be capability to consume the smallest size of crabs (CW 10 mm) commonly released in lakes and ponds, whereas at least 72.6 cm total length or 63.4 mm GW would be capability to consume all sizes of crabs (CW 34 mm) in these trails. Prey-size selection The prey-size selection for small (14.1–15.9 mm), medium (18.0–19.9 mm) and large (22.1~23.9 mm) crabs by three size classes of snakehead is shown in Fig. 2. All size classes of snakehead showed a rather high preference for small size crab than medium and large size crab (Tukey HSD test; P < 0.001), whereas no difference existed between medium and large size prey (Tukey HSD test; P = 0.325). Small size snakehead showed low preference for medium and large size crab (PI = 0.05; PI = 0) in all of 15 feeding trails,
1.2 Crab size Medium

Where ai is the preference index for prey size i, ri and pi is the proportion of prey size i consumed by predator and be presented in trail pools, m is the number of prey size class (m is 3 in these trails). Levene’s test was employed to check homogeneity of variances, if P > 0.05, then data were analyzed using two-way ANOVAS to determine whether prey size or predator size signi?cantly affected the preference of three size groups. Prey-size selection data were also analyzed using an honestly signi?cant difference test (HSD Tukey’s test) to detect differences in prey-size or predator-size groups. Oneway ANOVA test was used to determine differences of crab weight consumed by predator under three common carp weight levels. Prey type selection of snakehead was analyzed using paired-samples ttest. PI were log(x + 1) transformed prior to analysis, whereas prey weights were square root transformed to satisfy the assumptions of ANOVA. The signi?cance level used was P < 0.05. SPSS statistical software v13.0 was used for all statistical analyses. Results

1.0

Small

Large

Preference index

0.8

0.6

0.4

0.2

0.0

Maximum handling size The maximum handling size of predator feeding on crabs was both signi?cantly (P < 0.01) related to LT and GW (Fig. 1). The curves were ?tted by: (a) maximum handling size (M) = 3.238 + 0.424 LT (n = 19, r2 = 0.749) and (b) M = ?6.422 + 0.638 GW (n = 19, r2 = 0.839). The maximum handling size of crabs monotonically increased with

Small

Medium

Large

Predator size
Figure 2 Preference index by three size groups of snakehead (predator) when fed on three size groups of Chinese mitten crab. Predator size (LT) groups: small, 351–373 mm; medium, 433–458 mm; large, 582– 603 mm. Prey size (carapace width) groups: small, 14.1–15.9 mm; medium, 18.0–19.9 mm; large, 22.1– 23.9 mm.

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Prey weight consumed (g)

thus medium and large size predator displayed comparatively high selectivity for prey of medium and large size (Fig. 2). This suggests that preference index for medium and large size prey tends to increase by predator size. The preference index was signi?cantly affected by prey size and prey size 9 predator size interaction, however, was not affected by predator size (Table 3). Prey type selection Snakehead consumed higher proportions of crucian carp than crab, when two preys were presented simultaneously (Fig. 3). This suggests that Snakehead has a relatively high preference of crucian carp than crab, even crucian carp weight level was low. Crab weight consumed by predator monotonically decreased with crucian carp weight levels (One-way ANOVA, F2,6 = 26.807, P = 0.001). There was statistically signi?cant difference between crab and crucian carp captured by snakehead in all 63 feeding trails (regardless of crucian carp weight levels), using paired-samples t-test (t = 1.931, d.f. = 8, P = 0.045). Discussion Maximum handling size In our study, the maximum handling size of crab that could be consumed by snakehead monotonically increased with LT, thus a line regression model adapted to describe the relationship. This is in accordance with models of redear run?sh Lepomis microlophus feeding on Physa gyrina and Helisoma trivolvis, two common aquaculture-pond snails, which observed in Midwestern U.S. ponds and investigated by Wang, Hayward and Whitledge (2003). However, this result contrasts with the result of ?eld experiments, analyzed stomach contents of 598 red drum collected from Galveston

300 Crucian crap 250 Crab

200

150

100

50

0

0g

20 g

50 g

Crucian carp weight level

Figure 3 The in?uence of three different crucian carp weight levels on prey weight consumed accumulatively by the snakehead.

Table 3 Results of two-way ANOVAS analysis of the effects of prey and predator sizes on preference index of snakehead for three size classes of crab
Factor
Prey size Predator size Prey size 9 predator size

MS
0.123 0.002 0.024

F
84.135 1.032 16.219

d.f.
2,42 2,42 4,42

P
<0.001 0.367 <0.001

Bay, Scharf and Schlicht (2000) suggested that no change in maximum size of prey (blue crab Callinectes sapidus, white shrimp Penaeus setiferus and gulf menhaden Brevoortia patronus) consumed with increasing red drum size, but only a slight increase in mean size with increasing red drum size. Eklo ¨v and Diehl (1994) argued that this phenomenon is related to search mode of the predator. In addition, Brown and Haight (1992) argued that maximum prey size can also be in?uenced by the hunger level of the predator. The optimal foraging models for ?sh suggested that a forager maximizes net energy intake per unit time, and display high preference for prey sizes that can be best captured and handled (Werner & Hall 1974; Charnov 1976; Mittelbach 1981; Pyke 1984). Hence, the data of the maximum handling-size of prey can be consumed by predators from ?eld trails may be not the real ‘maximum size’, should be smaller than the truth maximum value probable. Our linear regression equation relating maximum handling size of Chinese mitten crab to snakehead LT will be useful for predicting safe spectrum of crab to snakehead of given size. Snakehead dominant maximum total length is smaller than 50 cm in many lakes of Changjiang River areas (Ma et al. 1997; Tan 1997; Xie et al. 1997; Zhang et al. 1999; Yu et al. 2008), by calculating with this equation, we suggest that the Chinese mitten crabs which CW larger than 24.4 mm will be safe for predation of snakehead.

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Gape size The maximum handling-size of prey that a predator can feed on is constrained by predator’s feeding apparatus (speci?cally the size of mouth gape) (Nilsson & Bro ¨ nmark 2000; Do ¨ rner & Wagner 2003; Holly & Thomas 2005), which we also found in our study. Furthermore, we found that the correlation index of predator’s GW and maximum handling-size of crab is signi?cantly different from predator’s LT and maximum handling-size of crab. The ratio of maximum handling-size of prey to LT of predator varied by prey type: piscivorous feeding on ?sh always larger than 50% (Scharf et al. 1998; Do ¨ rner & Wagner 2003; Holly & Thomas 2005); piscivorous feeding on snails less than 10% (Wang et al. 2003); snakehead feeding on juvenile Chinese mitten crab in our trails less than 5%. In comparison, the ratio of maximum handling size of prey to gape width of predator seems not varied acutely by prey type: Round gobies Neogobius melanostomus Pallas and alewives Alosa pseudoharengus Wilson consumed by yellow perch Perca ?avescens Mitchell were 53% and 46% respectively (Truemper & Lauer 2005); snakehead feeding on juvenile Chinese mitten crab in our trails was 58%. Therefore, we presume that GW of predator may be a more exactly criteria for predicting the maximum handling size of prey that could be consumed by predator of given size. Prey-size selection When given a choice of three sizes of crabs, all size classes of snakehead showed a rather high preference for small crab than medium and large size. It was a strong selection for small prey sizes by young of the year blue?sh Pomatomus saltatrix when presented a series sizes of Atlantic silverside Menidia menidia (Juanes & Conover 1994). Similarly, in ?eld situations, length frequencies of round goby and alewives consumed by yellow perch were signi?cantly smaller than those theoretically possible based on gape size and availability (Truemper & Lauer 2005). Juanes and Conover (1994) argued that all sizes of prey within the predator’s mouth gape are attacked as encountered, but those most vulnerable are ingested most often, resulting in ‘apparent’ preferences (for small prey). By the standpoint of optimal foraging theory, although the ingestion of large prey is energetically more advantageous (Elliott & Hurley

2000), then there will cost more energy to capture and handle large prey than small one, which may probably counteracts the energetically advantage. Thus, the vulnerability of prey is always increased by predator’s size. This conclusion agrees with Sih and Moore’s (1990) suggestion that prey behaviour and vulnerability may be as important as predator choice in determining predator diets. However, smaller prey is never excluded from the diet because their relative high vulnerability (Juanes, Stouder, Fresh & Feller 1994). Our results support this standpoint that medium and large predator showed high preference for small crab than medium and large, thus simultaneous displayed comparatively high selectivity for prey of medium and large size. Prey type selection In prey type selection trails, snakehead showed a relatively high preference of crucian carp (frozen) than crab, consumption of crab was signi?cantly decreased with crucian carp weight levels. We suggest that living crap possess better swimming ability than crab, hence use frozen carp as prey will more reasonable for this trials. Previous studies have demonstrated that even subtle differences in prey behaviour and morphology can dramatically affect foraging relationships (Werner & Gilliam 1984). Wahl (1988) concluded that both increased prey body depth and the presence of spines have been shown to negatively affect piscivorous ?sh predator capture ef?ciencies. For instance, Scharf and Schlicht (2000) found that juvenile blue?sh had higher capture success on Atlantic silverside (being a slender-bodied, obligate schooling species that lacks well-developed ?n spines) compared with striped bass (being a deep-bodied, facultative schooling species with well-developed dorsal and anal ?n spines). For predator, the choice of a particular prey type is determined to a certain degree from the morphological characteristics of their feeding apparatus (Labropoulou & Eleftheriou 1997). However, the antipredation function of crab’s certain morphological characteristics were varied by predator species. For an example, blue crab was a more important component than any other ?sh prey of red drum diets in Galveston Bay (Frederick & Kurtis 2000), but in our experiments, snakehead showed a relatively higher consumption of ?sh prey (crucian carp) than crabs.

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Implications for stock enhancement Snakehead is one of the most common piscivorous ?sh exists in the lakes where Chinese mitten crab stocked in Changjiang River area. In our trails, the maximum handling size of snakehead feeding on crabs monotonically increased with predator LT and GW; snakehead showed a rather high preference for small size crab and crucian carp; and the consumption of crab was monotonically decreased with crucian carp weight levels. Consideration of the results, we suggest that snakehead is likely to be one of important predators on juvenile Chinese mitten crab, but the crabs with CW larger than 24.4 mm will be safe for predation of snakehead in many lakes of Changjiang River areas and enhancement of the ?sh prey abundance could be valid ways to decrease the mortality rate of the crabs stocked. Obviously, additional research is necessary to estimate the in?uence of predation by piscivorous ?sh on mortality rates of released organisms in stock enhancement. Acknowledgments The authors are grateful to Zhang Chaowen and Chen Shannan for encouragement and constructive comments, and the anonymous referees for reviewing the manuscript critically. This research was ?nancially supported by the National Natural Science Foundation of China (No. 30830025 and 30970553) and the R & D Project of the Ministry of Science and Technology of China (No. 2012BAD25B05 and 2012BAD25B08). References
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