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Cannibalism and Habitat Selection of Cultured Chinese Mitten Crab: Effects of Submerged Aquatic Vegetation with Different Nutritional and Refuge Values

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Cannibalism and Habitat Selection of Cultured Chinese Mitten Crab: Effects of Submerged Aquatic Vegetation with Different Nutritional and Refuge Values water Article Cannibalism and Habitat Selection of Cultured Chinese Mitten Crab: Effects of Submerged Aquatic Vegetation with Different Nutritional and Refuge Values Qingfei Zeng 1,*, Erik Jeppesen 2,3, Xiaohong Gu 1,*, Zhigang Mao 1 and Huihui Chen 1 1 State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China; [email protected] (Z.M.); [email protected] (H.C.) 2 Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600 Silkeborg, Denmark; [email protected] 3 Sino-Danish Centre for Education and Research, University of CAS, Beijing 100190, China * Correspondence: [email protected] (Q.Z.); [email protected] (X.G.) Received: 26 September 2018; Accepted: 26 October 2018; Published: 29 October 2018 Abstract: We examined the food preference of Chinese mitten crabs, Eriocheir sinensis (H. Milne Edwards, 1853), under food shortage, habitat choice in the presence of predators, and cannibalistic behavior by comparing their response to the popular culture plant Elodea nuttallii and the structurally more complex Myriophyllum verticillatum L. in a series of mesocosm experiments. Mitten crabs were found to consume and thus reduce the biomass of Elodea, whereas no negative impact on Myriophyllum biomass was recorded. In the absence of adult crabs, juveniles preferred to settle in Elodea habitats (appearance frequency among the plants: 64.2 ± 5.9%) but selected for Myriophyllum instead when adult crabs were present (appearance frequency among the plants: 59.5 ± 4.9%). The mortality rate of mitten crabs in the absence of plant shelter was higher under food shortage, primarily due to cannibalism. The proportion of molting crabs dying in the structurally more complex Myriophyllum habitats was significantly lower than in the less complex Elodea habitats, indicating that Myriophyllum provides better protection from cannibalistic behavior, likely due to its structurally more complex canopy. Stable isotope analyses of crab samples revealed a trophic shift in both δ13C and δ15N (Dδ13C: 2.2–4.0 ; Dδ15N: 1.5–2.8 ) during the experimental period. Significant positive correlations between bodyh mass and δ13C andhδ15N were recorded, suggesting that cannibalistic feeding might further increase crab growth and lead to ontogenetic increases in trophic position with increasing size. Our study overall demonstrates that a combination of submerged aquatic vegetation functioning as a highly suitable food with other less palatable plant species acting as efficient refuges against predators may be the optimal method of plant stocking in mitten crab aquacultures to ensure both high crab growth and a high survival rate. Keywords: cannibalistic behavior; Elodea nuttallii; Myriophyllum verticillatum L.; crab culture; stable isotope 1. Introduction Cannibalism occurs frequently in natural and cultured populations of decapod crustaceans [1,2] and inter-cohort cannibalism plays a major role in controlling population size and structure [3]. Various factors may influence the extent and rate of cannibalism, including: (1) food availability [4,5], (2) crustacean density [6–9], (3) habitat structural complexity [2,10], and (4) prey vulnerability [7,11]. During ecdysis, crustaceans are especially vulnerable to predation and/or cannibalism [11,12]. Water 2018, 10, 1542; doi:10.3390/w10111542 www.mdpi.com/journal/water Water 2018, 10, x FOR PEER REVIEW 2 of 14 Water 2018, 10, 1542 2 of 14 [7,11]. During ecdysis, crustaceans are especially vulnerable to predation and/or cannibalism [11,12]. Numerous predator-prey studies have demonstrated that habitat complexity significantlysignificantly reduces the effects effects of of cannibalism cannibalism [2,6,7,13,14] [2,6,7,13,14 ]and and the the pr presenceesence of ofmultiple multiple shelters shelters has has been been shown shown to proportionallyto proportionally increase increase the the survival survival of ofjuvenile juvenile blue-swimmer blue-swimmer crabs, crabs, PortunusPortunus pelagicus pelagicus [1].[1]. Furthermore, both blue king crab, Paralithodes platypus ,, and red king crab, Paralithodes camtschaticus ,, have demonstrateddemonstrated a preferencea preference for complexfor complex habitats habi [6tats,7,15 [6,7,15].]. Moreover, Moreover, investigations investigations have revealed have revealedthat the ratesthat ofthe cannibalism rates of cannibalism of Age-1 redof Age-1 king crab red onking Age-0 crab specimens on Age-0 decreasedspecimens in decreased macroalgae in macroalgaerefuges [13, 14refuges]. A high [13,14]. refuge A high effect refuge seems effect to, therefore, seems to, reduce therefore, predator reduce movement predator andmovement aggressive and aggressiveactivity, increase activity, the increase duration the of resting,duration and of allowresting, the and prey allow to move the verticallyprey to move and horizontallyvertically and to horizontallyavoid predation to avoid [7,16 ,predation17]. [7,16,17]. Chinese mitten crab, Eriocheir sinensis (H.(H. Milne Edwards 1853), is an invasive species in North America and and Europe, Europe, and and due due to to the the generally generally low low concentration concentration of heavy of heavy metals metals in these in these areas, areas, it is intensivelyit is intensively fished fished for consumption, for consumption, which which contributes contributes to the tocontrol the control of populations. of populations. In China, In China,Japan, Korea,Japan, Korea,and other and parts other of parts the world, of the mitten world, crab mitten is regarded crab is regarded as a delicacy as a delicacy because because of its high of itsquality high andquality tasty and flesh, tasty and flesh, it andis, therefore, it is, therefore, of great of greatcomme commercialrcial value value [18]. [ 18In]. China, In China, the theyield yield and and value value of theof the species species have have grown grown steeply steeply from from 1991 1991 to 2015, to 2015, from from 8.4 8.4× 10×3 t10 in3 1991t in 1991 to 8.2 to × 8.2 105× t in10 52015,t in 2015,with withan estimated an estimated value value of 6.0 of 6.0× 10×7 10United7 United States States Dollars Dollars (USD) (USD) in in1991 1991 to to 6.5 6.5 ×× 10109 9USDUSD in in 2015 2015 [19] [19] (Figure1 ).1). However, However, extensive extensive mortality mortality occurring occurrin in theg in period the fromperiod stocking from stocking to harvesting, to harvesting, especially especiallyduring the during early stages the ofearly development, stages of hasdevelopm diminishedent, has the yieldsdiminished of cultivated the yields populations of cultivated [2,20], populationsand field studies [2,20], have and shown field studies that cannibalism have shown is a majorthat cannibalism problem in is the a commercialmajor problem production in the commercialof Chinese mittenproduction crabs. of Aquaculture Chinese mitten systems crabs. are Aquaculture characterized systems by high are stocking characterized densities, by lack high of stockingalternative densities, live food, lack and of absencealternative of naturallive food, refuges and absence [21], all of conditions natural refuges that are [21], likely all toconditions promote thatcannibalism. are likely Manyto promote studies cannibalism. of marine crabsMany suggest studies thatof marine the presence crabs suggest of suitable that sheltersthe presence for the of suitableintermolt shelters and/or for newly the moltedintermolt crabs and/or may decreasenewly molted the cannibalism crabs may [1 ,decrease2]. Yet, so the far, cannibalism only a few studies [1,2]. Yet,have so specifically far, only a addressed few studies the have cannibalistic specifically behavior addressed of freshwater the cannibalistic mitten crab behavior and how of submergedfreshwater mittenvegetation crab affects and how interspecific submerged interactions vegetation [18 affe,20cts,22 interspecific]. interactions [18,20,22]. × 4 × 8 Figure 1. Trends inin thethe productionproduction ( (×1010 4 t) and valuevalue ((×10108 UnitedUnited States States Dollars Dollars (USD)) (USD)) of Chinese mitten crab cultures from 1991 to 2015 in China (b (basedased on data from FAO (Food and Agriculture Organization of the United Nations) 2016 and ChinaChina fisheryfishery statisticsstatistics yearbooksyearbooks fromfrom 20122012 toto 2016).2016). Macrophytes serve as both a natural food source and a refuge for mitten crabs during molting [18]. Macrophytes serve as both a natural food source and a refuge for mitten crabs during molting At present, Elodea nuttallii is usually planted in the middle and lower reaches of the Yangtze River [18]. At present, Elodea nuttallii is usually planted in the middle and lower reaches of the Yangtze for mitten crab production due to its high colonization ability and faster growth under eutrophic River for mitten crab production due to its high colonization ability and faster growth under conditions [23,24]. Myriophyllum verticillatum L. is used less frequently in crab aquacultures; its more eutrophic conditions [23,24]. Myriophyllum verticillatum L. is used less frequently in crab finely dissected leaves compared to those of Elodea may increase the structural complexity of the habitat aquacultures; its more finely dissected leaves compared to those of Elodea may increase the Water 2018, 10, 1542 3 of 14 and thus act as a refuge, more than Elodea, for young crabs from cannibalism [25]. However, it is not well known how the two plants affect the intraspecific interaction and habitat choice of the crabs.
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