Abstract
Neptunea cumingii is an important nutrition-rich economic species in China. Juveniles of N. cumingii suffer from high mortality at low temperatures, which has proved a limiting factor in raising seedlings in artificial habitats. Previous research has shown that N. cumingii displays aggregation behavior in response to adverse environmental changes. Therefore, we determined the effects of temperature, food, size of juvenile snails, substratum type, and density of juvenile snails on the aggregation behavior of N. cumingii. Results show that, at a low (4°C) or a high (22°C) temperature, juvenile snails adjusted to the inhospitable environment by exhibiting increased aggregation behavior. However, their aggregation behaviors differed at these two temperatures. There was no significant difference in the aggregation rate, but the typical aggregation size was larger at 4°C than at 22°C. At 10°C or 16°C, aggregation behavior of juvenile snails reduced. Aggregation increased in the satiation treatment at 10°C and 16°C. Small-sized juveniles tended to have higher aggregation rates (92.22%) and a larger typical aggregation size. More juveniles were distributed in the bottom of shaded substrata. A larger typical aggregation size or higher density significantly reduced the mortality of juvenile snails at a low temperature (4°C). These results broaden our understanding of gastropod aggregation behavior and can be used to develop and improve commercial breeding strategies and resource recovery for N. cumingii.
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Data Availability Statement
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ancel A, Visser H, Handrich Y, Masman D, Le Maho Y. 1997. Energy saving in huddling penguins. Nature, 385(6614): 304–305, https://doi.org/10.1038/385304a0.
Batchelder P, Kinney R O, Demlow L, Lynch C B. 1983. Effects of temperature and social interactions on huddling behavior in Mus musculus. Physiology & Behavior, 31(1): 97–102, https://doi.org/10.1016/0031-9384(83)90102-6.
Cai Q H. 2001. Resource protection measures and processing methods of Naptunea cumingii. China Fisheries, (10): 73, https://doi.org/10.3969/j.issn.1002-6681.2001.10.051. (in Chinese)
Chapperon C, Seuront L. 2012. Keeping warm in the cold: on the thermal benefits of aggregation behaviour in an intertidal ectotherm. Journal of Thermal Biology, 37(8): 640–647, https://doi.org/10.1016/j.jtherbio.2012.08.001.
Clark B R, Faeth S H. 1997. The consequences of larval aggregation in the butterfly Chlosyne lacinia. Ecological Entomology, 22(4): 408–415, https://doi.org/10.1046/j.1365-2311.1997.00091.X.
Gilbert C, Blanc S, Giroud S, Trabalon M, Le Maho Y, Perret M, Ancel A. 2007. Role of huddling on the energetic of growth in a newborn altricial mammal. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 293(2): R867–R876, https://doi.org/10.1152/ajpregu.00081.2007.
Gilbert C, McCafferty D, Le Maho Y, Martrette J M, Giroud S, Blanc S, Ancel A. 2010. One for all and all for one: the energetic benefits of huddling in endotherms. Biological Reviews, 85(3): 545–569, https://doi.org/10.1111/j.1469-185X.2009.00115.X.
Hagen N T, Mann K H. 1994. Experimental analysis of factors influencing the aggregating behaviour of the green sea urchin Strongylocentrotus droebachiensis (Müller). Journal of Experimental Marine Biology and Ecology, 176(1): 107–126, https://doi.org/10.1016/0022-0981(94)90200-3.
Hatle J D, Salazar B A. 2001. Aposematic coloration of gregarious insects can delay predation by an ambush predator. Environmental Entomology, 30(1): 51–54, https://doi.org/10.1603/0046-225X-30.1.51.
Jarman P J. 1974. The social organisation of antelope in relation to their ecology. Behaviour, 48(1–4): 215–267, https://doi.org/10.1163/156853974X00345.
Kobak J, Poznańska M, Kakareko T. 2009. Effect of attachment status and aggregation on the behaviour of the zebra mussel Dreissena polymorpha. Journal of Molluscan Studies, 75(2): 119–126, https://doi.org/10.1093/mollus/eyn046.
Kotze J, Bennett N C, Scantlebury M. 2008. The energetics of huddling in two species of mole-rat (Rodentia: bathyergidae). Physiology & Behavior, 93(1–2): 215–221, https://doi.org/10.1016/j.physbeh.2007.08.016.
Lapointe V, Sainte-Marie B. 1992. Currents, predators, and the aggregation of the gastropod Buccinum undatum around bait. Marine Ecology Progress Series, 85: 245–257, https://doi.org/10.3354/meps085245.
Mehner T, Wieser W. 1994. Energetics and metabolic correlates of starvation in juvenile perch (Perca fluviatilis). Journal of Fish Biology, 45(2): 325–333, https://doi.org/10.1111/j.1095-8649.1994.tb01311.x.
Miao Z Q, Liu Z H, Xu J L, Zhou H B, Yan X J. 2016. Effects of light intensity on growth of juvenile Sinonovacula constricta (Lamarck, 1818). Journal of Ningbo University (Natural Science & Engineering Edition), 29(2): 1–5. (in Chinese with English abstract)
Miranda R M, Fujinaga K, Ilano A S, Nakao S. 2009. Effects of imposex and parasite infection on the reproductive features of the Neptune whelk Neptunea arthritica. Marine Biology Research, 5(3): 268–277, https://doi.org/10.1080/17451000802419422.
Miranda R M, Lombardo R C, Goshima S. 2008. Copulation behaviour of Neptunea arthritica: baseline considerations on broodstocks as the first step for seed production technology development. Aquaculture Research, 39(3): 283–290, https://doi.org/10.1111/j.1365-2109.2008.01901.x.
Nowack J, Geiser F. 2016. Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals. Journal of Experimental Biology, 219(4): 590–596, https://doi.org/10.1242/jeb.128926.
Rojas J M, Castillo S B, Escobar J B, Shinen J L, Bozinovic F. 2013. Huddling up in a dry environment: the physiological benefits of aggregation in an intertidal gastropod. Marine Biology, 160(5): 1 119–1 126, https://doi.org/10.1007/s00227-012-2164-6.
Scheibling R E, Lauzon-Guay J-S. 2007. Feeding aggregations of sea stars (Asterias spp. and Henricia sanguinolenta) associated with sea urchin (Strongylocentrotus droebachiensis) grazing fronts in Nova Scotia. Marine biology, 151(3): 1 175–1 183, https://doi.org/10.1007/s00227-006-0562-3.
Su Y L, Lu Z Z, Song J, Miao W. 2007. Effect of overwintering aggregation on energy metabolism in the firebug, Pyrrhocoris apterus (Heteroptera: pyrrhocoridae). Acta Entomologica Sinica, 50(12): 1 300–1 303, https://doi.org/10.3321/j.issn:0454-6296.2007.12.014. (in Chinese with English abstract)
Sukhchuluun G, Zhang X Y, Chi Q S, Wang D H. 2018. Huddling conserves energy, decreases core body temperature, but increases activity in Brandt’s voles (Lasiopodomys brandtii). Frontiers in Physiology, 9: 563, https://doi.org/10.3389/fphys.2018.00563.
Tojo S, Nagase Y, Filippi L. 2005. Reduction of respiration rates by forming aggregations in diapausing adults of the shield bug, Parastrachia japonensis. Journal of Insect Physiology, 51(10): 1 075–1 082, https://doi.org/10.1016/j.jinsphys.2005.05.006.
Xu J K, Peng L H, Gao W, Shen H D, Liang X, Yang J L. 2017. Effects of light intensity, water temperature and density on aggregation of juvenile mussel Mytilus coruscus. Journal of Dalian Ocean University, 32(3): 275–279, https://doi.org/10.16535/j.cnki.dlhyxb.2017.03.004. (in Chinese with English abstract)
Yoder J A, Hobbs III H H, Hazelton M C. 2002. Aggregate protection against dehydration in adult females of the cave cricket, Hadenoecus cumberlandicus (Orthoptera, Rhaphidophoridae). Journal of Cave and Karst Studies, 64(2): 140–144.
Zhang X F, Yang D Z, Zhou Y B, Yue Z H, Zhang L X, Xu K. 2014. Impacts of temperature and salinity on oxygen consumption rate and ammonia excretion rate in juvenile whelk Neptunea cumingii. Journal of Dalian Ocean University, 29(3): 251–255, https://doi.org/10.3969/J.ISSN.2095-1388.2014.03.010. (in Chinese with English abstract)
Zhang X Y, Sukhchuluun G, Bo T B, Chi Q S, Yang J J, Chen B, Zhang L, Wang D H. 2018. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome, 6(1): 103, https://doi.org/10.1186/s40168-018-0473-9.
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Supported by the National Key R&D Program of China (No. 2019YFD0900800), the fund earmarked for the Modern Agro-industry Technology Research System (No. CARS-49), the Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (No. 2019JZZY020708), the Industry Leading Talents Project of Taishan Scholars (to ZHANG Tao), the Double-Hundred Blue Industry Leader Team of Yantai (to ZHANG Tao), the Construction Technology and Demonstration Application of Dandong Characteristic Beach Type Marine Ranch (No. KFJ-STS-QYZD-189), the Shandong Peninsula Coastal Area Ecological Simulation Test Project: Marine Ranch Resource Evaluation and Sustainable Utilization Model Research; NSFC-Shandong Joint Fund for Marine Science Research Centers (No. U1406403), and the Creative Team Project of the Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology (No. LMEES-CTSP-2018-1)
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Yu, Z., Hu, Z., Song, H. et al. Aggregation behavior of juvenile Neptunea cumingii and effects on seed production. J. Ocean. Limnol. 38, 1590–1598 (2020). https://doi.org/10.1007/s00343-020-0042-5
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DOI: https://doi.org/10.1007/s00343-020-0042-5