Endocrine Function in Aquatic Invertebrates and Evidence for Disruption by Environmental Pollutants

Pinder, L. C. V.; Pottinger, T. G.; Billinghurst, Z.; Depledge, M. H.. 1999 Endocrine Function in Aquatic Invertebrates and Evidence for Disruption by Environmental Pollutants. Bristol, Environment Agency, 147pp. (R&D Technical Report E67, IFE Report no. WI/T11068I7/1)

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EXECUTIVE SUMMARY Objectives 1. This report addresses five primary objectives:- (i) to summarize the key elements of invertebrate endocrine systems; (ii) to assess whether existing test systems are adequate for the detection of endocrine disruption in invertebrates, what new tests might be required, which species of invertebrates are most appropriate for such tests, what end-points should be measured and whether the same organisms can be used for both laboratory and environmental monitoring; (iii) to review the published evidence for endocrine disruption in aquatic invertebrates (marine and freshwater; experimental and field studies) resulting from exposure to chemicals in the environment; (iv) to summarize the relevant UK and European legislation impacting on the monitoring and management of freshwater ecosystems; (v) to highlight the major gaps in knowledge and present an outline research programme to improve our understanding of the processes underpinning endocrine disruption in invertebrates. Endocrinology of invertebrates 2. The current state of understanding of the endocrinology of the major invertebrate groups has been summarised. It is clear that utilisation of hormones to control and coordinate biochemical, physiological and behavioural processes is common to all major invertebrate taxa. Neuropeptide signalling mechanisms which utilise the peptide products of specialised neurosecretory cells are the predominant effectors among the endocrine systems so far characterised in invertebrates. However, non-peptide endocrine messengers are also important in many groups. Both of these systems are potentially “at risk” from interference by disruptive contaminants. 3. Among the aquatic invertebrate taxa the endocrine systems of the two major arthropod classes, insects and crustaceans, are best documented. In addition to peptide hormones, insects utilise homosesquiterpenoid epoxides (the juvenile hormones) and ecdysteroids (ecdysone, 20-hydroxyecdysone), neither of which are found in vertebrates. A range of vertebrate-type steroids (androgens, estrogens, progestogens, corticosteroids) have been detected in insects but it remains to be proven whether these have a functional role. A similar situation occurs in the crustacea which possess a wide range of peptide hormones and also utilise ecdysteroids. In addition to ecdysteroids, the non-peptide methyl farnesoate acts as a hormone in crustacea. As is the case with insects, although vertebrate-type steroids are detected in crustacean tissues their functional significance is yet to be confirmed. 4. Although not as well documented as for arthropods, the endocrine systems of the molluscs have been extensively studied. Molluscs utilise a wide range of peptide hormones to control and coordinate major processes. In contrast to the arthropods, ecdysteroids do not appear to play an important role in molluscs. The presence of vertebrate-type steroids has been reported for a number of molluscan species and in some cases the evidence that these steroids play a functional role is strong. 5. Evidence for a significant role of vertebrate-type steroids is strongest within the echinoderms. In addition to peptide signalling and the use of the purine 1-methyladenine in the later stages of oocyte development, there is considerable published evidence suggesting that vertebrate-type steroids are synthesised by echinoderms and may have a role in the control of growth and reproduction. 6. For the remaining groups considered within the review (the Coelenterata, Porifera, Acoelomata, Aschelminthes and Annelida) there are varying degrees of understanding of endocrine-type processes and isolated reports of steroid synthesising activity. 7. If concerns regarding possible avenues for endocrine disruption in invertebrates are focused on non-peptide systems, it is clear that all invertebrate groups must be considered at risk or potentially susceptible to interference at a sub-lethal level by chemicals in the aquatic environment. However, given the complex and multi-functional nature of the role of those non-peptide hormones whose functions are best understood in invertebrates, the likely impact of interference at any particular locus within the endocrine system is difficult to predict. It is probable that effects of disruption will encompass reproduction, moulting, feeding, and behaviour. Regulatory Issues 8. Legislation and guidelines, relevant to the control of endocrine substances in the environment in Europe and North America, are reviewed. Ecotoxicological testing 9. The development of bioassays and biomarkers to assess endocrine disruption in aquatic invertebrates is, in principle, feasible. However, there appears to be no imperative for the development of wholly novel test systems. Uncertainty regarding the function of the endocrine system in many invertebrate species and a lack of understanding of the identity and possible sites of action of endocrine-disrupting chemicals precludes the development and application of cellular and subcellular screens for endocrine disrupting activity in invertebrates. The greatest benefits may be obtained by modifying the end-points of, or carrying out more detailed assessments in, existing test protocols. 10. Invertebrate test organisms provide the ability to monitor entire life cycles more readily than is the case for vertebrates, offering the prospect that integrative effects of exposure to potential endocrine disrupters can be detected more readily than is the case for vertebrates. Given the difficulties being encountered in relating cellular-level, or receptor-level, effects to whole-animal consequences by those working with endocrine disrupters in vertebrates, this may be an advantage, not a disadvantage. Clearly, invertebrates with short generation times offer the possibility of examining transgenerational and population level effects. 11. Caution should be employed when ascribing adverse effects of contaminant exposure to disruption of endocrine processes. Relatively few cases of contaminant effects on vertebrate reproductive processes can be confidently ascribed to endocrine disruption and the term endocrine disruption has been applied to cases where the biological/mechanistic basis for such effects is not established. This concern is exacerbated in the case of invertebrates where, in many cases, physiological and endocrine processes which may be affected are less well understood than is the case for many vertebrate species. Evidence for endocrine disrupting effects 12. A range of compounds with known endocrine-disrupting activity in invertebrates have been deliberately introduced into the environment and these frequently have been shown to have impacts on non-target species. Examples are the pesticides tebufenozide, a potent ecdysone agonist, and methoprene which is a juvenile hormone analogue. Tebufenozide is highly toxic to Cladocera, for which there is no apparent safe concentration, but surprisingly not to Copepoda. Methoprene is used in mosquito control and adversely affects reproductive performance of the crustacean Mysidopsis bahia at very low concentrations, probably through interference with the endogenous endocrine system. Effects have also been observed in a variety of other Crustacea but, as with Tebufenozide, susceptibility varies markedly, between taxa and life stages 13. A number of other pesticides, not specifically designed to interact with invertebrate hormonal systems also have effects, at low concentrations, that are suspected in some cases to be mediated through endocrine disruption. These include the herbicides atrazine, diquat and MCPA, the insecticides DDT and its derivatives, endosulfan and the biocide tributyltin (TBT). 14. Tributyltin is the best known endocrine disrupter in invertebrates having been identified as the agent responsible for global declines in populations of several molluscan species, through interference with reproduction. TBT is believed to inhibit the P-450-dependent aromatase responsible for conversion of testosterone to oestradiol-17. 15. The most commonly described effect of TBT exposure, termed imposex, is the imposition of male reproductive organs on the female of neogastropods. In some species, such as Nucella lapillus, this leads to the blocking of the female genital tract and consequent infertility. In some other closely related species infertility does not result from imposex, either because the underlying morphology prevents the female genital pore becoming blocked by the enlarged male organs or because the vulva elongates along with the growth of the penis and vas deferens. Worldwide, imposex has been reported to occur in 70 species of mollusc. There are few reports of imposex among freshwater molluscs but it has been reported from a tropical freshwater species, Marisa cornuarietis and reduced egg laying was noted in Biomphalaria glabrata when exposed to a very low concentration of TBT. 16. Sterilisation by less obvious means may occur in other molluscs when exposed to TBT. For example inhibition of larval production in the oyster Ostrea edulis may have been the result of hormonal retardation of the normal change from male to female during the reproductive cycle. 17. In the periwinkle Littorina littorea TBT exposure gives rise to development of the intersex condition through the development of male features in the female genital tract or supplanting of the female sex organs by those of the male. This is distinct from the imposex response shown by many neogastropods, where the male organs are superimposed on those of the female. A gradation of levels of response are evident, ranging from incomplete closure of the female genital tract to development of a seminal groove and small penis. No other signs of sex change or evidence of spermatogenesis have been identified. 18. Intersexuality is common in a number of crustaceans and is often associated with parasitic castration. However in harpacticoid copepods intersexuality is extremely rare. Unusually, a very high proportion of several species of harpacticoid have been found in the neighbourhood of the long-sea sewage outfall in the North Sea near Edinburgh. A causal relationship between this phenomenon and some form of chemical pollution is deemed to be a high possibility in this case. No effects were evident on community structure and all meiobenthic samples showed a high diversity of copepods. No traces of parasitism were detected.. Attempts to induce the effect in the laboratory using TBT were not successful. 19. A number of metals, notably cadmium, and PCBs are suspected of disrupting endocrine function in invertebrates. Cadmium and PCBs cause aberrations in the early development of the sea stars, Asterias rubens and Patiria miniata and the sea urchin Strongylocentrus intermedius. In male and female sea stars these chemicals cause significant reductions in the levels of progesterone and testosterone in the pyloric caeca and after prolonged exposure to PCBs elevated levels of testosterone were found in the testes and ovaries of sea stars. PCBs have also been shown to affect ovary growth and both cadmium and PCBs are believed to interfere with hormonal control of reproduction by steroids. 20. Colour changes in some crustaceans are regulated by pigment dispersing and pigment concentrating hormones. Both cadmium and a PCB, Aroclor 1242, inhibit the release of the black pigment dispersing hormone in the crab Uca pugilator. 21. Exposure of D magna to even very low concentrations of cadmium affects reproduction, apparently through interference with the endocytotic uptake of yolk by the oocytes. At slightly higher concentrations the intermoult period was also extended. Selenium has also been shown to inhibit or delay ecdysis. The role of ecdysteroids in crustacean reproduction is not properly understood but it seems that primary and secondary vitellogenesis are under ecdysteroid control, while 20-hydroxyecdysterone is well documented as having the major positive influence on the moulting cycle. 22. It has been hypothesised that the flexible cladoceran sex ratio may be more easily influenced by hormone-like xenobiotics than that of obligate sexual species leading to a prediction that the maximum frequency of males in any one year would have been higher before 1945. Data for Lake Mendota for 1895, 1975 and 1991 show a "dramatic" decrease in the frequency of males for 2 Daphnia species with time. 23. The oestrogenic insecticide endosulfan and the synthetic oestrogen diethylstilbestrol (DES) have no effect on sex differentiation in Daphnia magna but do influence reproductive success in this species. Chronic levels of exposure to DES also resulted in reduced moulting frequency. 24. The oestrogenic alkylphenol, 4-nonylphenol apparently reduces the rate of elimination of testosterone in D. magna, leading to accumulation of androgenic products and reduced fecundity of females. In recent research, in which D magna were exposed to p-tert-pentylphenol (PTP), some females showed conspicuous malformations of the carapace from which it appeared that they had undergone a form of external masculinization. 25. Production of eggs and females by Daphnia were both affected by exposure to nonylphenol though production of males was less sensitive. Similar effects also arose when females were exposed to a toxic strain of Microcystis (Cyanobacteria). 26. Plants produce chemicals known as phytoecdysteroids that are structurally very similar to the ecdysteroids of insects and crustaceans. These are very soluble in water and can compete with 20-hydroxyecdysone and so interfere with the ecdysteroid hormone system. Bioassays have demonstrated that many phytoecdysteroids exhibit moulting hormone activity in insects. Dragonflies exposed to paper- and pulp-mill (and tannery) effluent showed a shortened time to first moult and arrested moulting in the larvae, leading to a suggestion that the effluents contained juvenile hormone mimics. 27. Deformities in larvae of Chironomidae are associated with sediment contamination by heavy metals, phthalates and organochlorine pesticides and it is possible that these may result from disruption of hormone metabolism. If this is the case they could provide useful end-points for laboratory bioassay. More research is required in this field. 28. Endocrine mechanisms are responsible for organizing some types of invertebrate behaviour and further research in this area could also provide useful bioassay end-points. Research needs 29. An understanding of the endocrinology of relevant organisms is important if the mechanisms by which environmental contaminants elicit effects are to be accurately attributed. However, the detection of effects of exposure to contaminants in both natural and laboratory populations of invertebrates, and the assessment of the ability of chemicals to interfere with endocrine-dependent processes (growth, reproduction, behaviour), does not require a detailed understanding of the endocrinology of the organism concerned. Therefore, while undoubtedly important, research into the basic endocrinology of invertebrate species need not be considered a priority requirement. Existing research effort, which is driven by factors other than concerns arising from consideration of endocrine disruption, should be sustained and will continue to assist understanding within the field of invertebrate endocrine disruption. 30. It must be determined whether it is appropriate to instigate a test regime (or continue with existing test strategies) which identifies effects without necessarily identifying the route by which those effects occur, or whether it is important to discriminate between compounds which act via the endocrine system and those which do not. The former strategy involves the minimum of investment in new techniques and test methods, the latter strategy would require considerable investment in research to identify indicators of disruption in specific elements of the endocrine systems of a diverse range of invertebrate species. The most appropriate use of resources might encompass a dual track approach - continued testi

Item Type: Publication - Report
Programmes: CEH Programmes pre-2009 publications > Other
UKCEH and CEH Sections/Science Areas: _ Pre-2000 sections
ISBN: 1-873160-78-X
Funders/Sponsors: Environment Agency, Endocrine Modulators Steering Group
Additional Keywords: Invertebrates, steroid hormones, endocrine disruption, ecotoxicology, biomarkers
NORA Subject Terms: Marine Sciences
Biology and Microbiology
Ecology and Environment
Date made live: 27 Jul 2009 13:08 +0 (UTC)

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