AbstractPomacea canaliculata is one of the most successful invader in worldwide, adversely affecting native ecosystem through direct predation or indirect competition, while the mechanism of indirect effects on native species remain poorly understood. To clarify the effects of P. canaliculata on the native near-niche species, Bellamya purificata, a widespread freshwater gastropod in China, was selected as the research subject.

摘要福寿螺（Pomacea canaliculata）是世界上最成功的入侵者之一，通过直接捕食或间接竞争对当地生态系统产生不利影响，而对当地物种的间接影响机制仍知之甚少。为了阐明P.canaliculata对本地近生态位物种的影响，选择了中国广泛分布的淡水腹足类Bellamya purificata作为研究对象。

The changes of mortality, histology, antioxidant system as well as the intestinal flora diversity of B. purificata were explored in present study. The results showed that the median lethal dose of P. canaliculata culture solution for B. purificata was 23.76 ind/L and a concentration-dependent damage of both the gonad and hepatopancreas were observed, the gonadal villi were dissolved and the hepatopancreas cells were broken at 20 ind/L.

本研究探讨了B.purificata死亡率，组织学，抗氧化系统以及肠道菌群多样性的变化。结果表明，P.canaliculata培养液对B.purificata的半数致死剂量为23.76 ind/L，观察到性腺和肝胰腺的浓度依赖性损伤，性腺绒毛溶解，肝胰腺细胞在20 ind/L时破裂。

Furthermore, different concentrations of P. canaliculata culture solution leading to the antioxidant damage on the enzyme or non-enzyme systems of B. purificata at various degrees. Additionally, a decrease in the diversity of the intestinal flora was observed, accompanied by an increase in the abundance of pathogenic bacteria such as Pseudomonas and Aeromonas after the exposure of the culture solution of P.

此外，不同浓度的P.canaliculata培养液会导致不同程度的抗氧化损伤B.purificata的酶或非酶系统。此外，观察到肠道菌群多样性的减少，伴随着暴露于P的培养液后病原菌如假单胞菌和气单胞菌的丰度增加。

canaliculata. Last, after being recovered in freshwater for 24 h, the antioxidant damage of B. purificata and the disturbance of intestinal flora diversity were still not recovered especially in the high concentration group. The indirect competitive mechanism of P. canaliculata culture solution on B.

小管。最后，在淡水中恢复24小时后，B.purificata的抗氧化损伤和肠道菌群多样性的紊乱仍未恢复，特别是在高浓度组中。福寿螺培养液对B的间接竞争机制。

purificata were explored from the aspects of tissue, biochemical level and intestinal flora, which enriched the research of P. canaliculata invasion on native snails in China, and provided new insights for the study .

从组织、生化水平和肠道菌群等方面对纯化进行了探索，丰富了我国福寿螺入侵本地钉螺的研究，为研究提供了新的见解。

IntroductionBiological invasion is a serious ecological and environmental problem under the background of economic globalization, which is one of the five major global environmental problems of the twenty-first century1. Invasive species has caused significant economic losses in the invaded area2,3 and threaten the public health safety4, as well as the huge damage to biodiversity and ecosystem function5.

引言生物入侵是经济全球化背景下严重的生态和环境问题，是21世纪全球五大环境问题之一1。入侵物种在入侵地区造成了重大的经济损失2,3，威胁了公共卫生安全4，并对生物多样性和生态系统功能造成了巨大破坏5。

Pomacea canaliculata, is one of the most malignant invasive species worldwide6, which was introduced into China in 1981, causing great ecological impact and economic losses. P. canaliculata has a higher tolerance to environmental conditions than other native snail species, resulting in its expansive ecological niche7.

福寿螺（Pomacea canaliculata）是世界上最恶性的入侵物种之一，1981年引入中国，造成了巨大的生态影响和经济损失。P、 小管比其他本地蜗牛物种对环境条件的耐受性更高，因此其生态位广阔7。

A study has shown that P. canaliculata can accumulate uric acid in allantoin as a non-enzymatic antioxidant to survive its aestivation8. Moreover, P. canaliculata has multiple escape strategies and can quickly respond to predator pheromones or similar injured chemical signals9. After being attacked by predators, P.

一项研究表明，P.canaliculata可以在尿囊素中积累尿酸，作为一种非酶抗氧化剂，以在其夏眠期间存活8。此外，P.canaliculata具有多种逃逸策略，可以快速响应捕食者信息素或类似的受损化学信号9。被捕食者攻击后，P。

canaliculata can quickly repair the broken shells by hemolymph10. These life-history strategies give them an absolute advantage in the ecosystem, facilitating the gradual proliferation of invasive species populations and exerting substantial pressure on other species, further leading to reduced agricultural crop production and loss of local biodiversity11,12.

小管可以通过溶血性H10快速修复破损的贝壳。这些生活史策略使它们在生态系统中具有绝对优势，促进了入侵物种种群的逐渐扩散，并对其他物种施加了巨大压力，进一步导致农作物产量下降和当地生物多样性丧失11,12。

P. canaliculata has the advantage of displacing native snail species in competition for food and space13. It has been reported that the food consumption and fecundity of P canaliculata invading the everglades in United States are higher than those of the native snail Pomacea paludosa14. The detrimental impact of P.

P、 小管具有在食物和空间竞争中取代本地蜗牛物种的优势13。据报道，入侵美国大沼泽地的P canaliculata的食物消耗和繁殖力高于本地蜗牛Pomacea paludosa14。P的不利影响。

canaliculata on aquatic plants in invasive areas has been extensively docume.

入侵地区水生植物上的小管已被广泛记录。

After 72 h of exposure to B. purificata, the mortality rate was 11.11% in the control group, 22.22% in 1 ind/L and 5 ind/L groups, 38.89% in 10 ind/L group, 44.44% in 20 ind/L group, and 88.89% in 40 ind/L and 80 ind/L groups.The concentration of P. canaliculata culture solution was logarithmically transformed and construct a nonlinear model with the death rate of B.

暴露于纯化双歧杆菌72小时后，对照组死亡率为11.11%，1 ind/L和5 ind/L组死亡率为22.22%，10 ind/L组死亡率为38.89%，20 ind/L组死亡率为44.44%，40 ind/L和80 ind/L组死亡率为88.89%。对P.canaliculata培养液的浓度进行对数变换，构建死亡率为B的非线性模型。

purificata by Four-parameter Logistic model method. The fitting curve was showed in Fig. 1, and the median lethal concentration (LC50) was 23.76 ind/L. After 72 h-exposure, the mortality of snail was increased with the culture solution concentrations of P. canaliculata, reaching a peak mortality at 80 ind/L (88.89%), only about 10% of the experimental individuals could survive under the high concentration of culture solution exposure.Fig.

通过四参数Logistic模型方法纯化。拟合曲线如图1所示，半数致死浓度（LC50）为23.76 ind/L。暴露72小时后，蜗牛的死亡率随着P.canaliculata培养液浓度的增加而增加，达到峰值死亡率为80 ind/L（88.89%），只有约10%的实验个体可以在高浓度的培养液暴露下存活。图。

1The effects of P. canaliculata culture solution on the death rate of B. purificata after exposed for 72 h.Full size imageEffect of P. canaliculata culture solution on histology in gonads and hepatopancreasAs shown in Fig. 2, the gonad of B. purificata was mainly composed of adipocytes, epithelial cell and placental tissues.

1 P.canaliculata培养液对暴露72小时后B.purificata死亡率的影响。全尺寸图像P.canaliculata培养液对性腺和肝胰腺组织学的影响如图2所示，B.purificata的性腺主要由脂肪细胞，上皮细胞和胎盘组织组成。

The adipocytes were enveloped by epithelial cells, and the placental tissues covered them. The fertilized eggs were attached to the placental tissues and developed into larvae before being discharged into the tissue cavity (Fig. 2). In the control group, the placental tissues were arranged tightly and the boundary between villus and adipocytes was clear (Fig. 2a).

脂肪细胞被上皮细胞包裹，胎盘组织覆盖它们。受精卵附着在胎盘组织上，发育成幼虫，然后排入组织腔（图2）。在对照组中，胎盘组织排列紧密，绒毛和脂肪细胞之间的边界清晰（图2a）。

After exposed in the culture solution of P. canaliculata, the adipocytes gradually evacuated under the treatment of P. canaliculata culture solution at 1 ind/L (Fig. 2b) and 5 ind/L (Fig. 2c), resulting in edema formation. Under the treatment of 5 ind/L and 10 ind/L group, the adipocytes in t.

暴露于P.canaliculata培养液中后，脂肪细胞在1 ind/L（图2b）和5 ind/L（图2c）的P.canaliculata培养液处理下逐渐撤离，导致水肿形成。在5 ind/L和10 ind/L组的治疗下，t中的脂肪细胞。

MDA content of B. purificata increased after treatment with P. canaliculata culture solution without significance (P > 0.05). After B. purificata was recovered in sterile water for 24 h, the amount of MDA varied among all concentration of culture fluid (P < 0. 05, F = 1.132), and the highest amount appeared in the recovery group of 10 ind/L (7.44 nmol/mg prot) (Fig. 4a).Fig.

用P.canaliculata培养液处理后，B.purificata的MDA含量增加，但无显着性（P＞0.05）。在无菌水中回收纯化双歧杆菌24小时后，MDA的量在所有浓度的培养液中变化（P<0.05，F=1.132），最高量出现在恢复组10 ind/L（7.44 nmol/mg prot）（图4a）。图。

4Antioxidant enzyme activity and lipid peroxidation of B. purificata in treatment and recovery group. (a) MDA. (b) SOD. (c) CAT. (d) GSH. Different concentrations of treatment group and control group were analyzed by ANOVA. Different capital letters represent significant differences between the treatment groups (P < 0.05), and different lowercase letters represent significant differences between the recovery groups (P < 0.05).

4治疗组和恢复组纯化双歧杆菌的抗氧化酶活性和脂质过氧化。（a） 丙二醛。（b） SOD。（c） 猫。（d） 谷胱甘肽。通过ANOVA分析不同浓度的治疗组和对照组。不同的大写字母代表治疗组之间的显着差异（P<0.05），不同的小写字母代表恢复组之间的显着差异（P<0.05）。

* Means the statistical differences P < 0.05 between the treatment group and recovery group, statistics by double-tailed paired samples Student ‘s t test.Full size imageSOD activity of B. purificata was inhibited in high concentration group at 10 ind/L and 20 ind/L, and there was a significant difference between the control group to 10 ind/L group and 20 ind/L group (P < 0.05, F = 2.401).

*表示治疗组和恢复组之间的统计学差异P<0.05，通过双尾配对样本学生t检验进行统计。高浓度组在10 ind/L和20 ind/L时抑制了纯化双歧杆菌的全尺寸imageSOD活性，对照组与10 ind/L组和20 ind/L组之间存在显着差异（P<0.05，F=2.401）。

After recovered in sterile water for 24 h, the activity of SOD in control group was significantly higher than the 10 ind/L group and 20 ind/L (P < 0.05, F = 14.338) group and the activity of recovery group was significant lowered than the treatment group (P < 0.05). The activity of SOD in B. purificata hepatopancreas was inhibited after exposure to 10 and 20 ind/L culture solution of P.

在无菌水中恢复24小时后，对照组的SOD活性显着高于10 ind/L组和20 ind/L组（P<0.05，F=14.338），恢复组的活性显着低于治疗组（P<0.05）。暴露于10和20 ind/L的P培养液后，纯化双歧杆菌肝胰腺中SOD的活性受到抑制。

canaliculata, and this inhibition persisted after the disappearance of the stimulation source (Fig. 4b).After 72 h exposure to P. canaliculata culture solution, the highest CAT activity was observed in the tre.

小管，这种抑制作用在刺激源消失后持续存在（图4b）。暴露于P.canaliculata培养液72小时后，在tre中观察到最高的CAT活性。

Data availability

数据可用性

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

。

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Download referencesAcknowledgementsWe sincerely acknowledge Miss Na Li and Mr. Pengfei Ma for their their invaluable cooperation in preparing this research before they graduated from Dalian Ocean University.FundingThis study was funded by Modern Agro-industry Technology Research System (CARS-49), Innovation Support Program for High-level Talents of Dalian City (2019RD12), Basic scientific research project of Education Department of Liaoning province (LJKMZ20221107), Scientific Research Joint Fund of Liaoning Province (2023-MSLH-007), the Overseas Training Program for Innovation Team of Liaoning Province (201818), Innovation and Entrepreneurship Project for High-Level Talents of Dalian (2020RQ109), the Project of the Educational Department of Liaoning Province (No.

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LJ2020012), Laboratory Animal Domestication of Lampetra reissneri (JYTMS20231060).Author informationAuthors and AffiliationsLiaoning Normal University, Dalian, 116081, ChinaChangrun Sui, Mingyuan Liu, Shunqin Chuan & Jun LiKey Laboratory of Environment Controlled Aquaculture, Ministry of Education (Dalian Ocean University), Dalian, 116023, ChinaBaolong Wang, Tao Zhang, Weixiao Zhang, Ruipin Huang, Zhujun Qiu, Yuqing Wang, Wenyu Zhao & Qian ZhangZhejiang University, Hangzhou, 310030, ChinaYing LiuAuthorsChangrun SuiView author publicationsYou can also search for this author in.

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PubMed Google ScholarContributionsAll the authors have contributed to the conception and design of the study. Dr. Q.Z. and J.L. proposed the initial idea of this study. C.S. and M.L. conducted the experimental design and completed the main experiment of this study. The first draft of this manuscript was written by C.S.

PubMed谷歌学术贡献所有作者都为这项研究的概念和设计做出了贡献。Q.Z.博士和J.L.提出了这项研究的初步想法。C、 S.和M.L.进行了实验设计并完成了本研究的主要实验。这份手稿的初稿是由C.S.写的。

S.C., B.W. and T.Z. made figures in the manuscript. S.C., R.H. and W.Z. were responsible for the statistical analysis of the data. Y.W., W.Z. and Z.Q. searched and checked the references and proofread all the words in the manuscript. Sponsorship support for this study was provided by Professor Y.L., Dr.

S、 C.，B.W.和T.Z.在手稿中绘制了数字。S、 C.，R.H.和W.Z.负责数据的统计分析。Y、 W.，W.Z.和Z.Q.搜索并检查了参考文献，并校对了手稿中的所有单词。这项研究的赞助支持由Y.L.教授提供。

Q.Z. and Dr. J.L. Before the manuscript was uploaded, all authors have already read the manuscript and expressed their opinions. All authors read and approved the final manuscript.Corresponding authorsCorrespondence to.

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Qian Zhang or Jun Li.Ethics declarations

钱章或李军。道德宣言

Competing interests

相互竞争的利益

All authors declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled, “Responses of survival, antioxidant system and intestinal microbiota of native snail Bellamya purificata to the invasive snail Pomacea canaliculata”..

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Reprints and permissionsAbout this articleCite this articleSui, C., Liu, M., Chuan, S. et al. Responses of survival, antioxidant system and intestinal microbiota of native snail Bellamya purificata to the invasive snail Pomacea canaliculata.

转载和许可本文引用本文Sui，C.，Liu，M.，Chuan，S。等人。天然蜗牛Bellamya purificata的存活，抗氧化系统和肠道微生物群对入侵蜗牛福寿螺的反应。

Sci Rep 14, 21267 (2024). https://doi.org/10.1038/s41598-024-71520-1Download citationReceived: 20 March 2024Accepted: 28 August 2024Published: 11 September 2024DOI: https://doi.org/10.1038/s41598-024-71520-1Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

科学报告1421267（2024）。https://doi.org/10.1038/s41598-024-71520-1Download引文接收日期：2024年3月20日接受日期：2024年8月28日发布日期：2024年9月11日OI：https://doi.org/10.1038/s41598-024-71520-1Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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Keywords

关键词

Pomacea canaliculata

卡纳利苹果

Invasion mechanismHistological damageAntioxidant systemIntestinal microbiota

侵袭机制组织学损伤抗氧化系统肠道微生物群

Subjects

主题

BiochemistryCell biologyEcologyMicrobiologyZoology

生物化学细胞生物学生态学微生物学动物学

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