Nhiễm ký sinh trùng acanthocephalan làm tăng khả năng dung nạp deltamethrin của Gammarus roeselii (Giáp xác: Amphipoda)

Judith Kochmann1, Melanie Laier1, Sven Klimpel1, Arne N. Wick2, Uwe Kunkel2, Jörg Oehlmann3, Jonas Jourdan3
1Department of Integrative Parasitology and Zoophysiology, Goethe University of Frankfurt, Max-von-Laue-Straße 13, D-60438, Frankfurt am Main, Germany
2Federal Institute of Hydrology, Am Mainzer Tor 1, D-56068, Koblenz, Germany
3Department Aquatic Ecotoxicology, Goethe University of Frankfurt, Max-von-Laue-Straße 13, D-60438, Frankfurt am Main, Germany

Tóm tắt

Tóm tắtCác loài giáp xác amphipod đóng vai trò là ký chủ trung gian cho ký sinh trùng và đồng thời là những chỉ thị nhạy bén về ô nhiễm môi trường trong hệ sinh thái nước. Mức độ mà sự tương tác với ký sinh trùng ảnh hưởng đến khả năng tồn tại của chúng trong các hệ sinh thái ô nhiễm vẫn chưa được hiểu rõ. Trong nghiên cứu này, chúng tôi đã so sánh sự nhiễm trùng của Gammarus roeselii với hai loài Acanthocephala, Pomphorhynchus laevisPolymorphus minutus, dọc theo một gradient ô nhiễm trong khu vực đô thị Rhine-Main của Frankfurt am Main, Đức. Tỉ lệ nhiễm P. laevis rất thấp ở những khu vực thượng nguồn không ô nhiễm (P ≤ 3%), trong khi tỉ lệ nhiễm cao hơn (P ≤ 73%) và cường độ lên đến 9 cá thể được tìm thấy ở khu vực hạ nguồn—gần một điểm xả thải của một nhà máy xử lý nước thải lớn (WWTP). Sự nhiễm trùng đồng thời của P. minutusP. laevis xảy ra ở 11 cá thể. Tỉ lệ nhiễm cao nhất của P. minutusP ≤ 9% và một ký sinh trùng mỗi ký chủ giáp xác là cường độ tối đa ghi nhận được. Để đánh giá xem liệu việc nhiễm trùng có ảnh hưởng đến khả năng sống sót trong các môi trường ô nhiễm hay không, chúng tôi đã thử nghiệm độ nhạy của các amphipod nhiễm trùng và không nhiễm trùng đối với thuốc trừ sâu pyrethroid deltamethrin. Chúng tôi phát hiện ra sự khác biệt về độ nhạy phụ thuộc vào sự nhiễm trùng trong 72 giờ đầu tiên, với nồng độ hiệu ứng (24h EC50) là 49.8 ng/l và 26.6 ng/l đối với G. roeselii nhiễm trùng và không nhiễm trùng, tương ứng. Trong khi số lượng ký chủ cuối cùng có thể một phần giải thích cho tỉ lệ nhiễm cao của P. laevis trong G. roeselii, các kết quả từ bài thử nghiệm độc tính cấp tính gợi ý rằng việc nhiễm trùng acanthocephalan có tác động tích cực đến G. roeselii ở những khu vực ô nhiễm. Việc tích tụ mạnh mẽ chất ô nhiễm trong ký sinh trùng có thể đóng vai trò như một bể chứa cho sự tiếp xúc với thuốc trừ sâu của ký chủ. Do thiếu lịch sử đồng tiến hóa giữa ký sinh trùng và ký chủ cũng như thiếu sự thao túng hành vi (khác với các loài gammarid đã tiến hóa cùng nhau), nguy cơ bị động vật ăn thịt bởi cá vẫn không thay đổi, giải thích cho tỉ lệ nhiễm cao tại địa phương. Do đó, nghiên cứu của chúng tôi minh họa cách tương tác giữa các sinh vật có thể thúc đẩy khả năng tồn tại của một loài dưới sự ô nhiễm hóa học.

Từ khóa


Tài liệu tham khảo

Adam O, Degiorgi F, Crini G, Badot P-M (2010) High sensitivity of Gammarus sp. juveniles to deltamethrin: Outcomes for risk assessment. Ecotoxicol Environ Saf 73:1402–1407. https://doi.org/10.1016/j.ecoenv.2010.02.011

Bauer A, Trouvé S, Grégoire A, et al (2000) Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behavior of native and invader gammarid species. Int J Parasitol 5

Beckers L-M, Busch W, Krauss M et al (2018) Characterization and risk assessment of seasonal and weather dynamics in organic pollutant mixtures from discharge of a separate sewer system. Water Res 135:122–133. https://doi.org/10.1016/j.watres.2018.02.002

Bernhardt ES, Rosi EJ, Gessner MO (2017) Synthetic chemicals as agents of global change. Front Ecol Environ 15:84–90. https://doi.org/10.1002/fee.1450

Birk S, Chapman D, Carvalho L et al (2020) Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nat Ecol Evol 4:1060–1068. https://doi.org/10.1038/s41559-020-1216-4

Borgmann U (1996) Systematic analysis of aqueous ion requirements of Hyalella azteca: A standard artificial medium including the essential bromide ion. Arch Environ Contam Toxicol 30:356–363. https://doi.org/10.1007/BF00212294

Brettschneider DJ, Misovic A, Schulte-Oehlmann U et al (2019) Detection of chemically induced ecotoxicological effects in rivers of the Nidda catchment (Hessen, Germany) and development of an ecotoxicological, Water Framework Directive–compliant assessment system. Environ Sci Eur 31:7. https://doi.org/10.1186/s12302-019-0190-4

Brown AF, Pascoe D (1989) Parasitism and host sensitivity to cadmium: an acanthocephalan infection of the freshwater amphipod Gammarus pulex. J Appl Ecol 26:473–487. https://doi.org/10.2307/2404075

Bundschuh M, Gergs R, Schadt S, Schulz R (2013) Do differences in sensitivity between native and invasive amphipods explain their coexistence in Lake Constance? A case study with lambda-cyhalothrin. Chemosphere 92:483–489. https://doi.org/10.1016/j.chemosphere.2013.01.106

Busch MW, Kuhn T, Münster J, Klimpel S (2012) Marine crustaceans as potential hosts and vectors for metazoan parasites. In: Mehlhorn H (ed) Arthropods as Vectors of Emerging Diseases. Springer, Berlin, Heidelberg, pp 329–360

Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575. https://doi.org/10.2307/3284227

Cramp S (1977) Handbook of the Birds of Europe the Middle East and North Africa. The Birds of the Western Palearctic. Vol. I: Ostrich to Ducks. Oxford: Oxford University Press. pp. 78–89. ISBN 978–0–19–857358–6

Csapó H, Krzywoźniak P, Grabowski M et al (2020) Successful post-glacial colonization of Europe by single lineage of freshwater amphipod from its Pannonian Plio-Pleistocene diversification hotspot. Sci Rep 10:18695. https://doi.org/10.1038/s41598-020-75568-7

Dangles O, Malmqvist B (2004) Species richness–decomposition relationships depend on species dominance. Ecol Lett 7:395–402. https://doi.org/10.1111/j.1461-0248.2004.00591.x

Davies T, Field L, Usherwood P, Williamson M (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59(3):151–162. https://doi.org/10.1080/15216540701352042

Dezfuli BS, Rossetti E, Bellettato CM, Maynard BJ (1999) Pomphorhynchus laevis in its intermediate host Echinogammarus stammeri in the River Brenta, Italy. J Helminthol 73:95–102. https://doi.org/10.1017/S0022149X99000153

Domisch S, Amatulli G, Jetz W (2015) Near-global freshwater-specific environmental variables for biodiversity analyses in 1 km resolution. Scientific data 2, S. 150073. https://doi.org/10.1038/sdata.2015.73.

Dorts J, Silvestre F, Tu HT et al (2009) Oxidative stress, protein carbonylation and heat shock proteins in the black tiger shrimp, Penaeus monodon, following exposure to endosulfan and deltamethrin. Environ Toxicol Pharmacol 28:302–310. https://doi.org/10.1016/j.etap.2009.05.006

Emde S, Kochmann J, Kuhn T et al (2014) Getting what is served? Feeding ecology influencing parasite-host interactions in invasive round goby Neogobius melanostomus. PLOS ONE 9:e109971. https://doi.org/10.1371/journal.pone.0109971

Ford A, Ågerstrand M, Brooks B, et al (2021) The role of behavioral ecotoxicology in environmental protection. Environ Sci Technolhttps://doi.org/10.1021/acs.est.0c06493

Frank SN, Godehardt S, Nachev M et al (2013) Influence of the cestode Ligula intestinalis and the acanthocephalan Polymorphus minutus on levels of heat shock proteins (HSP70) and metallothioneins in their fish and crustacean intermediate hosts. Environ Pollut Barking Essex 180:173–179. https://doi.org/10.1016/j.envpol.2013.05.014

Fuchs S, Ziegler S, Wander R (2018) ReWaM - Verbundprojekt NiddaMan: Entwicklung eines nachhaltigen Wasserressourcen-Managements am Beispiel des Einzugsgebiets der Nidda: Schlussbericht: Teilprojekt 5 - Szenarienentwicklung und Modellierung. Karlsruher Institut für Technologie (KIT). Karlsruhe. https://doi.org/10.2314/GBV:1034724274.

German Surface Water Ordinance (2016). Verordnung zum Schutz der Oberflächengewässer (Oberflächengewässerverordnung - OGewV). Anlage 9: Anforderungen an Analysenmethoden, an Laboratorien und an die Beurteilung der Überwachungsergebnisse. Bundesgesetzblatt I 2016: 1432–1433. https://www.gesetze-im-internet.de/ogewv_2016/anlage_9.html

Giari L, Fano EA, Castaldelli G et al (2020) The ecological importance of amphipod–parasite associations for aquatic ecosystems. Water 12:2429. https://doi.org/10.3390/w12092429

Gilbert BM, Avenant-Oldewage A (2017) Parasites and pollution: the effectiveness of tiny organisms in assessing the quality of aquatic ecosystems, with a focus on Africa. Environ Sci Pollut Res Int 24:18742–18769. https://doi.org/10.1007/s11356-017-9481-8

Gismondi E, Cossu-Leguille C, Beisel J-N (2012) Acanthocephalan parasites: help or burden in gammarid amphipods exposed to cadmium? Ecotoxicology 21:1188–1193. https://doi.org/10.1007/s10646-012-0873-8

Golvan YJ (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi 1801): L’ordre des Paleacanthocephala Meyer 1931 – La superfamille des Echinorynchoidea (Cobbold 1876) Golvan et Houin (1963). Muséum national d’Histoire naturelle, Paris, 373p. (Mémoires du Muséum national d’Histoire naturelle, Sér. A – Zoologie (1950–1992); 57)

Grabner D, Sures B (2019) Amphipod parasites may bias results of ecotoxicological research. Dis Aquat Organ 136:121–132. https://doi.org/10.3354/dao03355

Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams – a review. Int Rev Hydrobiol 86:383–393. https://doi.org/10.1002/1522-2632(200107)86:4/5%3c383::AID-IROH383%3e3.0.CO;2-D

Grethlein M, Pelikan L, Dombrowski A, Kabus J, Oehlmann J, Weigand A, Jourdan J (2022) Small-scale population structuring results in differential susceptibility to pesticide exposure. Environ Sci Eur 34:113

Hermes N, Jewell KS, Wick A, Ternes TA (2018) Quantification of more than 150 micropollutants including transformation products in aqueous samples by liquid chromatography-tandem mass spectrometry using scheduled multiple reaction monitoring. J Chromatogr A 1531:64–73. https://doi.org/10.1016/j.chroma.2017.11.020

Jackson DA, Peres-Neto PR, Olden JD (2011) What controls who is where in freshwater fish communities the roles of biotic, abiotic, and spatial factors. Can J Fish Aquat Scihttps://doi.org/10.1139/f00-239

Jackson MC, Loewen CJG, Vinebrooke RD, Chimimba CT (2016) Net effects of multiple stressors in freshwater ecosystems: a meta-analysis. Glob Change Biol 22:180–189. https://doi.org/10.1111/gcb.13028

Jażdżewski K (1980) Range extensions of some gammaridean species in European inland waters caused by human activity. Crustac Suppl 84–107

Jourdan J, Krause ST, Lazar VM et al (2016) Shared and unique patterns of phenotypic diversification along a stream gradient in two congeneric species. Sci Rep 6:38971. https://doi.org/10.1038/srep38971

Jourdan J, Piro K, Weigand A, Plath M (2019) Small-scale phenotypic differentiation along complex stream gradients in a non-native amphipod. Front Zool 16:29. https://doi.org/10.1186/s12983-019-0327-8

Kelly D, Paterson R, Townsend C, Poulin R, Tompkins D (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

Kennedy CR (2006) Ecology of the Acanthocephala, 1st edition. Cambridge University Press, Cambridge; New York

Kidd H, James D (eds) (1991) The agrochemicals handbook. The Royal Society of Chemistry, Unwin, Old Working, Surrey, U.K.

Labaude S (2016) Effect of the environment on the interaction between gammarids (Crustacea: Amphipoda) and their manipulative acanthocephalan parasites. Unpublished PhD Thesis. http://rgdoi.net/10.13140/RG.2.2.33921.25443

Leuven RSEW, van der Velde G, Baijens I et al (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biol Invasions 11:1989. https://doi.org/10.1007/s10530-009-9491-7

Loewe S, Muischnek H (1926) Über Kombinationswirkungen. Naunyn-Schmiedebergs Arch Für Exp Pathol Pharmakol 114:313–326. https://doi.org/10.1007/BF01952257

Lucius R, Loos-Frank B, Lane, RP (2018) Biologie von Parasiten. 3. Edition. Berlin, Heidelberg: Springer Spektrum

Lu Q, Sun Y, Ares I et al (2019) Deltamethrin toxicity: A review of oxidative stress and metabolism. Environ Res 170:260–281. https://doi.org/10.1016/j.envres.2018.12.045

Marcogliese DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1:151–164. https://doi.org/10.1007/s10393-004-0028-3

Matthews WJ (1998) Patterns in freshwater fish ecology, 1998th edn. Springer, New York

McCahon C, Brown AF, Pascoe D (1988) The effect of the acanthocephalan Pomphorhynchus laevis (Müller 1776) on the acute toxicity of cadmium to its intermediate host, the amphipod Gammarus pulex (L.). https://doi.org/10.1007/BF01056030

McCahon CP, Poulton MJ (1991) Lethal and sub-lethal effects of acid, aluminium and lime on Gammarus pulex during repeated simulated episodes in a Welsh stream. Freshw Biol 25:169–178. https://doi.org/10.1111/j.1365-2427.1991.tb00482.x

Médoc V, Rigaud T, Motreuil S et al (2011) Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98:825–835. https://doi.org/10.1007/s00114-011-0831-y

Mehlhorn H, Piekarski G (2002) Grundriss der Parasitenkunde - Parasiten des Menschen und der Nutztiere. Spektrum, 6th edition: 1–516

Molbert N, Alliot F, Leroux-Coyau M et al (2020) Potential benefits of acanthocephalan parasites for chub hosts in polluted environments. Environ Sci Technol 54:5540–5549. https://doi.org/10.1021/acs.est.0c00177

Moret Y, Bollache L, Wattier R, Rigaud T (2007) Is the host or the parasite the most locally adapted in an amphipod–acanthocephalan relationship? A case study in a biological invasion context. Int J Parasitol 37:637–644. https://doi.org/10.1016/j.ijpara.2006.12.006

Munz NA, Burdon FJ, de Zwart D et al (2017) Pesticides drive risk of micropollutants in wastewater-impacted streams during low flow conditions. Water Res 110:366–377. https://doi.org/10.1016/j.watres.2016.11.001

Nachev M, Sures B (2016) Environmental parasitology: Parasites as accumulation bioindicators in the marine environment. J Sea Res 113:45–50. https://doi.org/10.1016/j.seares.2015.06.005

Nõges P, Argillier C, Borja Á et al (2016) Quantified biotic and abiotic responses to multiple stress in freshwater, marine and ground waters. Sci Total Environ 540:43–52. https://doi.org/10.1016/j.scitotenv.2015.06.045

Ohler K, Schreiner VC, Link M, Liess M, Schäfer RB (2022) Land use changes biomass and temporal patterns of insect cross‐ecosystem flows. Global Chang Biol. https://doi.org/10.1111/gcb.16462

Oliveira C, Almeida J, Guilhermino L et al (2012) Acute effects of deltamethrin on swimming velocity and biomarkers of the common prawn Palaemon serratus. Aquat Toxicol Amst Neth 124–125:209–216. https://doi.org/10.1016/j.aquatox.2012.08.010

Palmquist K, Salatas J, Fairbrother A. (2012) Pyrethroid insecticides: use, environmental fate, and ecotoxicology. In: Perveen F, editor. Insecticides-advances in integrated pest management, pp. 251–278.

Pawlisz AV, Busnarda J, McLauchlin A et al (1998) Canadian water quality guidelines for deltamethrin. Environ Toxicol Water Qual 13:175–210. https://doi.org/10.1002/(SICI)1098-2256(1998)13:3%3c175::AID-TOX1%3e3.0.CO;2-4

Pérez-Fernández V, García MÁ, Marina ML (2010) Characteristics and enantiomeric analysis of chiral pyrethroids. J Chromatogr A 1217:968–989. https://doi.org/10.1016/j.chroma.2009.10.069

Perrot-Minnot M-J (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54. https://doi.org/10.1016/j.ijpara.2003.10.005

Perrot-Minnot M-J, Bollache L, Lagrue C (2020) Distribution of Pomphorhynchus laevis s.l. (Acanthocephala) among fish species at a local scale: importance of fish biomass density. J Helminthol 94:e99. https://doi.org/10.1017/S0022149X1900097X

Perrot-Minnot M-J, Guyonnet E, Bollache L, Lagrue C (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. Int J Parasitol Parasites Wildl 8:135–144. https://doi.org/10.1016/j.ijppaw.2019.01.007

Perrot-Minnot M-J, Maddaleno M, Balourdet A, Cézilly F (2012) Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Funct Ecol 26:1007–1014. https://doi.org/10.1111/j.1365-2435.2012.02027.x

Persson L, Carney Almroth BM, Collins CD, et al (2022) Outside the safe operating space of the planetary boundary for novel entities. Environ Sci Technolhttps://doi.org/10.1021/acs.est.1c04158

Petersen RC, Cummins KW (1974) Leaf processing in a woodland stream*. Freshw Biol 4:343–368. https://doi.org/10.1111/j.1365-2427.1974.tb00103.x

Piscart C, Moreteau J-C, Beisel J-N (2005) Biodiversity and structure of macroinvertebrate communities along a small permanent salinity gradient (Meurthe River, France). Hydrobiologia 551:227–236. https://doi.org/10.1007/s10750-005-4463-0

Poulin R (1999) The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29:903–914. https://doi.org/10.1016/s0020-7519(99)00045-4

Prenter J, MacNeil C, Dick JTA et al (2004) Lethal and sublethal toxicity of ammonia to native, invasive, and parasitised freshwater amphipods. Water Res 38:2847–2850. https://doi.org/10.1016/j.watres.2004.03.042

R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

Rigaud T, Moret Y (2003) Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitologyhttps://doi.org/10.1017/S0031182003004050

Ritz C, Strebig JC, Ritz MC (2016) Package ‘drc’. Creative Commons: Mountain View, CA, USA.Rothe LE, Loeffler F, Gerhardt A, et al (2022) Parasite infection influences the biomarker response and locomotor activity of Gammarus fossarum exposed to conventionally-treated wastewater. Ecotoxicol Environ Saf 236:113474. https://doi.org/10.1016/j.ecoenv.2022.113474

Rothe LE, Loeffler F, Gerhardt A, Feld CK, Stift R, Weyand M, Grabner D, Sures B (2022) Parasite infection influences the biomarker response and locomotor activity of Gammarus fossarum exposed to conventionally-treated wastewater. EcotoxicolEnviron Saf 236:113474

Scheurer M, Storck FR, Graf C et al (2011) Correlation of six anthropogenic markers in wastewater, surface water, bank filtrate, and soil aquifer treatment. J Environ Monit JEM 13:966–973. https://doi.org/10.1039/c0em00701c

Schmidt G (1985) Development and life cycles. In: Crompton D, Nickol B (eds) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 273–305

Schmidt-Rhaesa, A (2015) Gastrotricha, Cycloneuralia and Gnathifera. Volume 3: Gastrotricha and Gnathifera. Berlin, Germany, Munich, Germany, Boston, Massachusetts: Walter de Gruyter GmbH (Handbook of Zoology)

Siddall R, Sures B (1998) Uptake of lead by Pomphorhynchus laevis cystacanths in Gammarus pulex and immature worms in chub (Leuciscus cephalus). Parasitol Res 84:573–577. https://doi.org/10.1007/s004360050451

Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34(1):77–96. https://doi.org/10.1146/annurev.en.34.010189.000453

Sures B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol 20:170–177. https://doi.org/10.1016/j.pt.2004.01.014

Sures B, Nachev M, Selbach C, Marcogliese DJ (2017) Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology.’ Parasit Vectors 10:65. https://doi.org/10.1186/s13071-017-2001-3

Sures B, Radszuweit H (2007) Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala). J Helminthol 81:191–197. https://doi.org/10.1017/S0022149X07751465

Sures B, Siddall R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Exp Parasitol. https://doi.org/10.1006/EXPR.1999.4437

Sures B, Taraschewski H, Jackwerth E (1994) Lead accumulation in Pomphorhynchus laevis and its host. J Parasitol 80:355–357. https://doi.org/10.2307/3283403

Torchin ME, Lafferty KD, Dobson AP et al (2003) Introduced species and their missing parasites. Nature 421:628–630. https://doi.org/10.1038/nature01346

Tucca F, Díaz-Jaramillo M, Cruz G et al (2014) Toxic effects of antiparasitic pesticides used by the salmon industry in the marine amphipod Monocorophium insidiosum. Arch Environ Contam Toxicol 67:139–148. https://doi.org/10.1007/s00244-014-0008-8

Wei T, Simko V (2021) R package 'corrplot': visualization of a correlation matrix. (Version 0.92), https://github.com/taiyun/corrplot.

Weigand AM, Michler-Kozma D, Kuemmerlen M, Jourdan J (2020) Substantial differences in genetic diversity and spatial structuring among (cryptic) amphipod species in a mountainous river basin. Freshw Biol 65:1641–1656. https://doi.org/10.1111/fwb.13529

Weston D, Lydy M (2010) Urban and agricultural sources of pyrethroid insecticides to the Sacramento-San Joaquin Delta of California. Environ Sci Technol 44:1833–1840. https://doi.org/10.1021/es9035573

Le Yen TT, Rijsdijk L, Sures B, Jan Hendriks A (2014) Accumulation of persistent organic pollutants in parasites. Chemosphere 108:145–151. https://doi.org/10.1016/j.chemosphere.2014.01.036

Zander CD (1998) Parasit-Wirt-Beziehungen – Einführung in die ökologische Parasitologie. Springer: 1–184