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Effects of Endocrine Disrupting Compounds and Temperature on the Moulting Frequency of the Freshwater Isopod Asellus Aquaticus L

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Effects of Endocrine Disrupting Compounds and Temperature on the Moulting Frequency of the Freshwater Isopod Asellus Aquaticus L Effects on the moulting frequency of Asellus aquaticus 105 ACTA BIOLOGICA BENRODIS 13 (2006): 105-115 Effects of endocrine disrupting compounds and temperature on the moulting frequency of the freshwater isopod Asellus aquaticus L. (Isopoda: Asellota)* Effekte von hormonähnlich wirksamen Substanzen und Temperatur auf die Häutungsfrequenz der Süßwasserassel Asellus aquaticus L. (Isopoda: Asellota) LENNART WELTJE 1, 2 & JÖRG OEHLMANN 2 1 International Graduate School (IHI), Ecotoxicology Group, Markt 23, D-02763 Zittau, Germany, [email protected], corresponding author 2 J.W. Goethe University, Department of Ecology and Evolution – Ecotoxicology, Siesmayerstraße 70, D-60323 Frankfurt am Main, Germany Summary: The effects of the vertebrate endocrine disrupting compounds diuron, linuron, vinclo- zolin (pesticides), 17α-ethinylestradiol and tamoxifen (pharmaceuticals) on the moulting frequen- cy of the freshwater isopod Asellus aquaticus (L.) are described. In addition, the influence of temperature on moulting frequency was studied. Since moulting is under the control of the steroid hormone 20-hydroxyecdysone, effects may be expected of substances known to influence the steroid sex hormones (i.e. estradiol and testosterone) of vertebrates. Although the chemicals induced changes in moulting frequency (both stimulating and inhibiting effects were found), significant differences were not established. At 20 ºC, the moulting frequency was higher than at 15 °C, but again the difference was not significant. Consequently, improvements in the experimental set-up are discussed. It is concluded that experiments are best performed at a constant temperature, with young, isolated individuals of similar size and sex. Pesticides, moulting frequency, Asellus aquaticus Zusammenfassung: Effekte der wirbeltierhormonähnlich wirksamen Substanzen Diuron, Linu- ron, Vinclozolin (Pflanzenschutzmittel), 17α-Ethinylöstradiol und Tamoxifen (Arzneimittel) auf die Häutungsfrequenz der Süßwasserassel Asellus aquaticus (L.) werden beschrieben. Zusätzlich wur- de der Einfluss der Temperatur auf die Häutungsfrequenz untersucht. Da die Häutung über das Steroidhormon 20-Hydroxyecdyson kontrolliert wird, können Effekte von Substanzen erwartet werden, von denen bekannt ist, dass sie die steroiden Sexualhormone von Vertebraten (d.h. Östradiol und Testosteron) beeinflussen. Obwohl die getesteten Chemikalien einen Einfluss auf die Häutungs- frequenz hatten (sowohl fördernde als auch hemmende Effekte wurden beobachtet), wurden keine signifikanten Unterschiede gefunden. Bei 20 °C war die Häutungsfrequenz höher als bei 15 °C, aber der Unterschied war ebenfalls nicht signifikant. Deshalb werden Verbesserungen des experimentellen Aufbaus diskutiert. Daraus wird geschlossen, dass die Versuche am besten bei konstanter Temperatur mit jungen, isolierten Individuen von gleicher Größe und Geschlecht durchgeführt werden. Pflanzenschutzmittel, Häutungsfrequenz, Asellus aquaticus * Contribution to the First European Workshop on Isopods, Düsseldorf 14.-16. November 2003, Germany ACTA BIOLOGICA BENRODIS 13 (2006) 106 LENNART WELTJE & JÖRG OEHLMANN 1. Introduction ca), but it has not been established that they fulfil a functional role (VANDENBERGH et 1.1. Endocrine disruptions in invertebrates al.2003; DEFUR et al. 1999). It may therefore be unrealistic to expect vertebrate xeno-estro- At present, research on the disruption of gens to have estrogenic effects in crustaceans, hormonal processes in animals is mainly fo- but they could affect other endocrine pro- cussed on vertebrates and on in vitro systems cesses, such as moulting (ZOU & FINGERMAN derived from them. The vertebrate endocrine 1997). A possible working mechanism for system is quite well understood and the char- such EDCs is an interaction with the ecdyste- acterisation of its steroid hormones and as- roid receptor, and for bisphenol A and 17α- sociated receptors is on a relatively high level. ethinylestradiol, ecdysteroid antagonistic ac- A fair number of recent in vivo studies with tivity has been shown in a Drosophila melano- chemicals known to interact with the verte- gaster cell line (DINAN et al. 2001). Further, MU brate endocrine system (particularly the xeno- & LEBLANC (2002) have shown that the devel- estrogens bisphenol A, 4-n-nonylphenol and opmental toxicity of testosterone to the 17α-ethinylestradiol), have also demonstrated crustacean Daphnia magna involves anti-ecdy- effects in invertebrates, including molluscs, steroidal activity. DE LOOF & HUYBRECHTS insects and crustaceans (BALDWIN et al. 1997; (1998) suggested in their review that ecdyste- BROWN et al. 1999; OEHLMANN et al. 2000; roids, which are also involved in vitellogen- HAHN et al. 2002; WATTS et al. 2002; VANDEN- esis, may function as the counterparts of ver- BERGH et al. 2003; this list is not exhaustive). tebrate sex steroids in insects. This implies The difficulty with most of these invertebrate that interactions of vertebrate EDCs with the studies is to unequivocally prove that the ef- ecdysteroid receptor may elicit (anti-)estrogenic fect shown is due to the disturbance of an type of effects, not per se related to the pres- endocrine mechanism and not, for instance, ence of an estrogen receptor. On the contrary, by general toxicity (SEGNER et al. 2003). How- other invertebrate groups, notably molluscs ever, such mechanistic proof is required, and echinoderms, do seem to have a func- since it forms the very basis by which an en- tional role for some vertebrate-type steroids, docrine disrupting compound (EDC) is de- hence working mechanisms similar to those fined. To gather this proof, a reasonable in vertebrates may apply. Finally, the experi- amount of knowledge should be available mental design often does not allow for a de- on the endocrinology of the organism under finitive conclusion on the (endocrine) wor- study. In the case of invertebrates, this know- king mechanism of a compound. Hence, ledge is often insufficient. many cases point towards a possibly endo- There are three main issues that hamper crine-mediated effect (e.g. increased reproduc- the interpretation of invertebrate EDC data: tive output, altered moulting behaviour, The first problem is the large diversity in endo- shifted sex-ratios), but evidence remains cir- crine mechanisms, hormones and processes, cumstantial. existing within the invertebrate world, which Although it is evident, from the meanwhile comprises about thirty phyla, against one ‘classic’ example of imposex in gastropods, single phylum of vertebrates (DEFUR et al. caused by organotin compounds, such as tri- 1999). Many mechanisms of endocrine con- butyltin (TBT) and triphenyltin (TPhT) (for trol are simply not known or not fully inves- an overview see CSTEE, 1999), that endocri- tigated yet. Secondly, vertebrate-type steroids ne disruption does occur in natural popula- (estradiol, testosterone, progesterone) have tions of invertebrates, they have not received been detected in a number of invertebrate the amount of attention they deserve within species, e.g. in higher crustaceans (Malacostra- the framework of EDC research. Especially Effects on the moulting frequency of Asellus aquaticus 107 if one considers that at least 95% of the 4) Crustaceans have readily measurable end- known animal species consists of inverte- points, such as moulting and regenerati- brates, which comprise keystone species for on, which are coupled processes under the functioning of ecosystems and food- neuroendocrine control (WEIS et al. 1992; webs, a greater effort should be undertaken FINGERMAN et al. 1998). to investigate to what extent endocrine dis- 5) A useful endpoint could be the forma- ruption really affects invertebrates. tion of oostegites in female isopods. Oo- stegites are ventral overlapping plates, 1.2. Isopods as model organisms to forming the marsupium or brood pouch, assess endocrine disruption which develop after a special moult, the so-called parturial moult, which preceeds Isopods belong to the higher crustaceans fertilisation. The latter can only take place (Malacostraca), the largest class of the sub- when the exoskeleton is still flexible in phylum Crustacea, which are part of the phy- the hours directly after moulting, and is lum Arthropoda. Insects are the other main the main reason why male aquatic isopods arthropod class, and in terms of species monopolize females by carrying them on numbers, arthropods are the most success- their ventral surface (a precopula behaviour ful group of invertebrates, hence important called mate guarding) (ZIMMER 2001). for global biodiversity research. Arthropods 6) Field evidence exists for abnormal sexual are a good starting point to investigate endo- development in amphipod (Malacostra- crine disruption for a number of reasons: ca) populations (GROSS et al. 2001; NA- 1) The endocrine system of insects is described GEL et al. 2002). Various degrees of inter- to a much greater extent than that of any sex have also been found in natural iso- other invertebrate group, mainly because of pod populations (see CHARNIAUX-COTTON the silkworm industry and pest control of 1960), but a relation with environmental insects (DEFUR et al. 1999). A substantial chemicals has not been established. part of the knowledge gathered on insects Isopods occupy key positions as decom- is also applicable to crustaceans. posers in freshwater, terrestrial and marine 2) Insect pest control initiated the develop- ecosystems and may thus provide sentinel ment of third generation pesticides, which
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