Elsevier

Chemosphere

Volume 53, Issue 8, December 2003, Pages 827-833
Chemosphere

Juvenile hormone agonists affect the occurrence of male Daphnia

https://doi.org/10.1016/S0045-6535(03)00761-6Get rights and content

Abstract

The water flea Daphnia magna reproduces primarily by cyclic parthenogenesis. Environmental stimuli that signal a change to adverse conditions induce the organisms to switch from parthenogenesis to gamogenetic reproduction. During the gamogenetic period, they produce male daphnids and dormant resting eggs, which can survive prolonged periods of environmental adversity. However, little is known about the mechanisms associated with the switch from parthenogenesis to gamogenetic reproduction. We investigated the effects of several juvenoids on sex determination in Daphnia. Females less than 24 h old were exposed to various concentrations of the test substance and were observed for 21 days. It was found that they can trigger the appearance of male daphnids: the percentage of males in the population increases to a level greater than what occurs under ordinary environmental conditions. We found that methylfarnesoate, juvenile hormone III, methoprene, and the phenoxyphenoxy derivatives pyriproxyfen and fenoxycarb (both insecticides) reduced the production of offspring and produced sex ratios dominated by male daphnids. Pyriproxyfen and fenoxycarb showed striking effects at low concentrations. Exposure to either of these chemicals at a concentration of 330 ng l−1 caused adult females to produce almost all male neonates. Methylfarnesoate, juvenile hormone III, and methoprene showed an effect in inducing male production at higher concentrations (3.7 × 103, 3.3 × 105, and 1.3  × 105 ng l−1, respectively). Our findings suggest that juvenile hormone agonists, including some insecticides, affect the chemical signaling responsible for inducing the production of male offspring.

Introduction

The water flea Daphnia magna (Cladocera, Crustacea) occupies an important position in aquatic food webs because it is a major part of the diet of fish and invertebrate predators. It also plays a major role in the control of water quality by feeding on algae (Dodson and Hanazato, 1995).

In general, daphnids reproduce by parthenogenesis, in which females asexually produce genetically identical female offspring. Because the parthenogenetic reproduction system provides rapid expansion of daphnid populations, a daphnid population consists almost entirely of females when resources are abundant. It is known that daphnids switch their reproductive strategy from parthenogenesis to gamogenesis (sexual reproduction) in response to environmental changes such as depletion of resources or crowding (Kleiven et al., 1992). After males are produced, sexual reproduction can occur, which has two major advantages. One is genetic recombination (Deng and Lynch, 1996), leading to greater genetic diversity, which could improve a daphnid population’s ability to adapt to changing environments. The other advantage is the production of resting eggs that can withstand severe environmental conditions, such as freezing temperatures or drought.

Although the change in reproductive strategy in daphnids is phenomenologically well known, little is known concerning the neuroendocrine factors that link the environmental stimuli to the ultimate biochemical and physiological responses that initiate the production of males (Baer and Owens, 1999). Recent studies have shown that sex determination in invertebrates can be influenced by toxicants. For example, exposure of daphnid populations to atrazine in the laboratory alters the sex ratio of the offspring (Dodson et al., 1999). Methoprene stimulates male offspring production and defers their production to later stages of the sexual reproductive period, while inhibiting the production of resting eggs and promoting the continuance of parthenogenetic reproduction (Olmstead and LeBlanc, 2001).

Methylfarnesoate and juvenile hormone III are juvenile hormones in crustaceans and insects, respectively (Laufer et al., 1993; Nijhout, 1994). Methoprene [isopropyl(E,E)-(R,S)-11-methoxy-3,7,11-trimethyldodeca-2,4-dienoate] is a juvenile hormone (JH) analog used to control mosquito populations by preventing larvae from metamorphosing into adults (Arias and Mulla, 1975). Insect JH analogs also include pyriproxyfen and fenoxycarb (Fig. 1). Pyriproxyfen [phenoxyphenoxy(R,S)-2-(2-pyridyloxy)propyl ether] is a juvenoid insect growth regulator used to control a wide range of insect pests, including mosquitoes (Estrada and Mulla, 1986) and chironomids (Ali et al., 1993). Fenoxycarb [ethyl 2-(4-phenoxyphenoxy)ethylcarbamate] is a carbamate insect growth regulator. It is used in baits for fire ants and for the control of fleas, mosquitoes, cockroaches, butterflies, moths, and scale insects. It is also used to control these pests on stored products (US Environmental Protection Agency, 1983–1985).

High concentrations of JH and low concentrations of molting hormone cause molting larvae to continue growing as larval instars. JH has two primary effects on insects: one is morphogenetic, that is, modulation of larval growth and development and inhibition of premature metamorphosis (Riddiford, 1996); the other is a gonadotrophic effect––regulation of several aspects of reproductive physiology including vitellogenesis (Koeppe and Ofengand, 1976).

Given that a JH analog, methoprene, affects the reproductive system of Daphnia and that some insecticides are JH analogs, it is natural that we should examine whether other JH analogs have the same effects on the reproductive strategy of Daphnia. We found that Daphnia exposed to JH and JH analogs produced more males than normal, indicating that these chemicals can be used to study the mechanisms involved in the transition from parthenogenesis to gamogenesis.

Section snippets

Materials and methods

Methylfarnesoate (all-trans, 90% pure) was provided by Dr. H. Sonobe (Konan University, Kobe, Japan), and it was synthesized by methylation of (2E,6E)-farnesoic acid (which was a gift of Kuraray Co. Ltd., Tokyo, Japan) with diazomethane according to a general methylation procedure (Monson, 1971). The synthetic methylfarnesoate was purified by silica gel chromatography (1.5% diethyl ether in pentane) followed by reverse-phase high-performance liquid chromatography (column; Wakosil 5C18, 150 mm × 

Juvenile hormone and its analogs reduce the number of offspring produced

In the present study, five juvenoids (methylfarnesoate, juvenile hormone III, methoprene, pyriproxyfen, and fenoxycarb) were tested for their effects on fecundity and sex determination in D. magna. Both pyriproxyfen and fenoxycarb reduced the total number of offspring at relatively low concentrations, 10–30 ng l−1 (Fig. 2). In contrast, methylfarnesoate, juvenile hormone III, and methoprene showed significant reduction of reproduction only at much higher concentrations (Fig. 2). Thus, the effect

Discussion

In the present study, we found that five juvenoids increased the percentage of males produced by exposed D. magna. Since the skewed sex ratio toward male on exposure to the chemicals was accompanied by reduced reproduction, there is a possibility that female-biased mortality rate gives rise to male-biased sex ratio. However, this possibility is rejected because daphnids usually produce only females under these assay conditions (i.e., fewer than 0.1% males for the strain we used) and male

Acknowledgments

We are grateful to Dr. Louis Guillette, University of Florida, for his encouragement and for critical reading of the manuscript. We thank Ms. Ryoko Abe and Mr. Masaaki Koshio for the assistance in the laboratory. Special thanks are due to Dr. H. Sonobe, who provided us with the synthesized methylfarnesoate. This work was supported in part by a Grant-in-Aid for Scientific Research of Priority Area (A) from the Ministry of Education, Sports, Culture, Science and Technology of Japan and by grants

Norihisa Tatarazako got his Ph.D. degree in Agriculture, from the University of Tokyo, Bunkyo-ku, Tokyo, Japan in November 2002. During April 1988–March 2001, he was an R&D engineer at Oji Pulp and Paper Co. Ginza, Tokyo, Japan. At this time, he studied about pulp and paper mill effluents and developed biological tests to evaluate environmental pollution. From April 2001 to till date, he is an R&D engineer at the National Institute for Environmental Studies, Tsukuba, Ibaraki, Japan. As a member

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Norihisa Tatarazako got his Ph.D. degree in Agriculture, from the University of Tokyo, Bunkyo-ku, Tokyo, Japan in November 2002. During April 1988–March 2001, he was an R&D engineer at Oji Pulp and Paper Co. Ginza, Tokyo, Japan. At this time, he studied about pulp and paper mill effluents and developed biological tests to evaluate environmental pollution. From April 2001 to till date, he is an R&D engineer at the National Institute for Environmental Studies, Tsukuba, Ibaraki, Japan. As a member and R&D engineer, he is studying endocrine-disrupting chemicals.

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