Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum

Amphipods are commonly parasitized by acanthocephalans and microsporidians and co-infections are found frequently. Both groups of parasites are known to have severe effects on their host. For example, microsporidians can modify host sex ratio and acanthocephalans can manipulate the behavior of the a...

Full description

Bibliographic Details
Main Authors: Hui-Yu Chen, Daniel S. Grabner, Milen Nachev, Hsiu-Hui Shih, Bernd Sures
Format: Article
Language:English
Published: PeerJ Inc. 2015-10-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/1353.pdf
_version_ 1797418864383885312
author Hui-Yu Chen
Daniel S. Grabner
Milen Nachev
Hsiu-Hui Shih
Bernd Sures
author_facet Hui-Yu Chen
Daniel S. Grabner
Milen Nachev
Hsiu-Hui Shih
Bernd Sures
author_sort Hui-Yu Chen
collection DOAJ
description Amphipods are commonly parasitized by acanthocephalans and microsporidians and co-infections are found frequently. Both groups of parasites are known to have severe effects on their host. For example, microsporidians can modify host sex ratio and acanthocephalans can manipulate the behavior of the amphipod to promote transmission to the final host. These effects influence host metabolism in general and will also affect the ability of amphipods to cope with additional stressors such as environmental pollution, e.g., by toxic metals. Here we tested the effects of sub-lethal concentrations of cadmium on glycogen and lipid levels, as well as on the 70kDa heat shock protein (hsp70) response of field collected Gammarus fossarum, which were naturally infected with microsporidians and the acanthocephalan Polymorphus minutus. Infected and uninfected G. fossarum were exposed to a nominal Cd concentration of 4 µg/L, which resembled measured aqueous Cd concentration of 2.9 µg/L in reconstituted water for 7 d at 15 °C in parallel to an unexposed control. After exposure gammarids were snap frozen, weighed, sexed and tested for microsporidian infection by PCR. Only individuals containing the microsporidian Dictyocoela duebenum were used for the further biochemical and metal analyses. P. minutus infected amphipods were significantly smaller than their uninfected conspecifics. Mortality was insignificantly increased due to cadmium exposure, but not due to parasite infection. Microsporidian infection in combination with cadmium exposure led to increased glycogen levels in female gammarids. An increase of glycogen was also found due to interaction of acanthocephalan and microsporidian infection. Elevated lipid levels were observed in all groups infected with microsporidians, while acanthocephalans had the opposite effect. A positive correlation of lipid and glycogen levels was observed. The general stress response measured in form of hsp70 was significantly increased in microsporidian infected gammarids exposed to cadmium. P. minutus did not affect the stress response of its host. Lipid levels were correlated negatively with hsp70 response, and indicated a possible increased stress susceptibility of individuals with depleted energy reserves. The results of our study clearly demonstrate the importance of parasitic infections, especially of microsporidians, for ecotoxicological research.
first_indexed 2024-03-09T06:39:10Z
format Article
id doaj.art-4df66d803a0944f6a083a77273cf2b0b
institution Directory Open Access Journal
issn 2167-8359
language English
last_indexed 2024-03-09T06:39:10Z
publishDate 2015-10-01
publisher PeerJ Inc.
record_format Article
series PeerJ
spelling doaj.art-4df66d803a0944f6a083a77273cf2b0b2023-12-03T10:52:56ZengPeerJ Inc.PeerJ2167-83592015-10-013e135310.7717/peerj.1353Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarumHui-Yu Chen0Daniel S. Grabner1Milen Nachev2Hsiu-Hui Shih3Bernd Sures4Department of Life Science, National Taiwan University, Taipei, TaiwanAquatic Ecology and Centre for Water and Environmental Research, University of Duisburg–Essen, Essen, GermanyAquatic Ecology and Centre for Water and Environmental Research, University of Duisburg–Essen, Essen, GermanyDepartment of Life Science, National Taiwan University, Taipei, TaiwanAquatic Ecology and Centre for Water and Environmental Research, University of Duisburg–Essen, Essen, GermanyAmphipods are commonly parasitized by acanthocephalans and microsporidians and co-infections are found frequently. Both groups of parasites are known to have severe effects on their host. For example, microsporidians can modify host sex ratio and acanthocephalans can manipulate the behavior of the amphipod to promote transmission to the final host. These effects influence host metabolism in general and will also affect the ability of amphipods to cope with additional stressors such as environmental pollution, e.g., by toxic metals. Here we tested the effects of sub-lethal concentrations of cadmium on glycogen and lipid levels, as well as on the 70kDa heat shock protein (hsp70) response of field collected Gammarus fossarum, which were naturally infected with microsporidians and the acanthocephalan Polymorphus minutus. Infected and uninfected G. fossarum were exposed to a nominal Cd concentration of 4 µg/L, which resembled measured aqueous Cd concentration of 2.9 µg/L in reconstituted water for 7 d at 15 °C in parallel to an unexposed control. After exposure gammarids were snap frozen, weighed, sexed and tested for microsporidian infection by PCR. Only individuals containing the microsporidian Dictyocoela duebenum were used for the further biochemical and metal analyses. P. minutus infected amphipods were significantly smaller than their uninfected conspecifics. Mortality was insignificantly increased due to cadmium exposure, but not due to parasite infection. Microsporidian infection in combination with cadmium exposure led to increased glycogen levels in female gammarids. An increase of glycogen was also found due to interaction of acanthocephalan and microsporidian infection. Elevated lipid levels were observed in all groups infected with microsporidians, while acanthocephalans had the opposite effect. A positive correlation of lipid and glycogen levels was observed. The general stress response measured in form of hsp70 was significantly increased in microsporidian infected gammarids exposed to cadmium. P. minutus did not affect the stress response of its host. Lipid levels were correlated negatively with hsp70 response, and indicated a possible increased stress susceptibility of individuals with depleted energy reserves. The results of our study clearly demonstrate the importance of parasitic infections, especially of microsporidians, for ecotoxicological research.https://peerj.com/articles/1353.pdfEcotoxicologyEnvironmental parasitologyMicrosporidiaAcanthocephalaEnergy reservesCystacanth
spellingShingle Hui-Yu Chen
Daniel S. Grabner
Milen Nachev
Hsiu-Hui Shih
Bernd Sures
Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
PeerJ
Ecotoxicology
Environmental parasitology
Microsporidia
Acanthocephala
Energy reserves
Cystacanth
title Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
title_full Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
title_fullStr Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
title_full_unstemmed Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
title_short Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum
title_sort effects of the acanthocephalan polymorphus minutus and the microsporidian dictyocoela duebenum on energy reserves and stress response of cadmium exposed gammarus fossarum
topic Ecotoxicology
Environmental parasitology
Microsporidia
Acanthocephala
Energy reserves
Cystacanth
url https://peerj.com/articles/1353.pdf
work_keys_str_mv AT huiyuchen effectsoftheacanthocephalanpolymorphusminutusandthemicrosporidiandictyocoeladuebenumonenergyreservesandstressresponseofcadmiumexposedgammarusfossarum
AT danielsgrabner effectsoftheacanthocephalanpolymorphusminutusandthemicrosporidiandictyocoeladuebenumonenergyreservesandstressresponseofcadmiumexposedgammarusfossarum
AT milennachev effectsoftheacanthocephalanpolymorphusminutusandthemicrosporidiandictyocoeladuebenumonenergyreservesandstressresponseofcadmiumexposedgammarusfossarum
AT hsiuhuishih effectsoftheacanthocephalanpolymorphusminutusandthemicrosporidiandictyocoeladuebenumonenergyreservesandstressresponseofcadmiumexposedgammarusfossarum
AT berndsures effectsoftheacanthocephalanpolymorphusminutusandthemicrosporidiandictyocoeladuebenumonenergyreservesandstressresponseofcadmiumexposedgammarusfossarum