FISHING NEWS OF THE WEIRD: Something strange is going on in our waters ... Some fish don't know whether they're boys or girls.
As my last blog as an NAFC staff editor, I''m going to focus on something a bit more serious and scientific than my typical tales of baitshops, antique lures and run-and-gun fishing.
If you would, let me hop on a soapbox and explore a phenomena that affects all anglers: signs that point to compromised fish reproduction in our waters—and how we owe a debt of gratitude to our beloved bait, the common fathead minnow, for helping scientists figure out what's going on.
To do so, I'll revisit a paper I wrote a couple of years ago while enrolled in Biology 4401/5401: Fish Physiology and Behavior at the University of Minnesota.
If you're thinking, great, this is gonna be a snooze, don't worry. I'll do my best to paraphrase the highfalutin academic-speak with something we can understand as fishermen.
Let's call it "Anglish."
To make it even easier on you, I'll italicize the grad school talk, so you can easily skip over it if you want.
I guess this blog is kind of a writing experiment ... about fisheries experiments. REAL Fishing News Of The Weird.
ABSTRACT
Over the past 15 years there has been a growing amount of research on the effects of endocrine disrupting chemicals (EDCs) on freshwater fish, wildlife and humans. Much of the research in the fields of ecotoxicology, fish physiology and behavior, and comparative biochemistry has utilized the fathead minnow (Pimephales promelas) as a sentinel species – a canary in the coal mine, so to speak – to indicate what greater impact these environmental factors may have on other species, including humans.
Results from numerous experiments throughout the world demonstrate that continued inputs of natural and synthetic estrogens and their mimics to aquatic environments in various municipal, industrial, and agricultural effluents could decrease the reproductive success and sustainability of fish populations.
In plain "Anglish": Via water and sewage treatment plants, farms and industrial sites, hormones and hormone-like compounds in water entering our lakes, rivers and streams could be seriously affecting the ability of gamefish to reproduce, drawing into question fish population sustainability.
One of the most significant observed physiological phenomena is the feminization of male fish in locations spanning the globe, including the United States, United Kingdom, continental Europe, and Japan, and most likely all points in between.
Again, in plain 'Anglish': Around the world, male fish are taking on female physiological characteristics.
This feminization has been linked to various levels of exposure to female hormones such as the natural estrogen17b-estradiol (E2) and the synthetic estrogen 17a-ethynylestradiol (EE2), both of which are not completely broken down by even the most sophisticated in-use municipal wastewater treatment plant (MWTP) processes. These estrogens – and estrogen mimics and xenoestrogens like alkylphenols, bisphenol A, and a host of other chemicals used in the manufacturing of industrial, agricultural, food, and pharmaceutical products – have been shown to cause dubious ecological impact.
'Anglish': Birth control and other forms of medication contain estrogens that simply cannot be completely removed from wastewater, whether by centrifuge or other means, although engineers are working diligently to fix this. That said, no matter our best practices in wastewater management, a certain amount of these chemicals (in varying amounts) do end up in our waterways. And they appear to be creating a phenomena called "intersexing." For example, this phenomena has been studied in populations of smallmouth bass in the Potomac River and its tributaries. Find out more here.
Hats Off To The Fathead
To measure potential implications of this intersexing phenomena, scientists have turned to the fathead minnow for its ease of use in the lab, its resiliency, and its representation of the largest family of freshwater fishes, Cyprinidae, which includes 2400 species of 220 genera. Not sure what they look like? Visit just about any baitshop in the country and you'll find something that resembles the fathead minnow in the photo below.
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| Fisherman's (and scientist's) friend – Pimephales promelas – the fathead minnow |
This paper (er, blog) reviews some of the wide range of scientific discourse on the effects of natural and synthetic estrogens on fathead minnows over the past decade. Specifically, it describes some of the common effects of these compounds on reproductive and endocrine physiology, provides a chronological summary of some of the major studies, explores some of the controversies and problems related to the topic, offers some interpretation and analysis, and finally, a temporary conclusion to what is in fact a burgeoning field of study.
Biomarkers For Estrogen Exposure
With respect to, but not limited to fathead reproductive physiology, there exist several biomarkers for estrogen exposure: 1) increased levels of VTG (egg yolk precursor protein) production during oogenesis in females; 2) increased levels of VTG in the liver and blood of males (typically unexpressed); 3) decreased levels of androgenic hormones testosterone and 11-ketotestosterone (KT) in males; 4) inhibition of gonadal development in both males and females; and, 5) inhibition of spermatogenesis. All studies on the effects of estrogens on fathead minnows address the above conditions as observed in the results of their respective experiments.
'Anglish': Exposure to these hormones affects both female and male fatheads. The females' sex organs mature later in their life-cycle than typical but when they do, they develop more egg protein. Likewise, the males' sex organs mature later in their life-cycle, they have lower testosterone levels and cannot produce sperm.
One of the seminal studies investigating the link between E2 levels in the aquatic environment and possible implications for ecological risk assessment was published in 1998 by a Michigan State University team of researchers who successfully provided a benchmark for determining the type and extent of substances that mimic the action of E2 via direct agonism of the estrogen receptor such as alkyl phenols1. They subjected fathead minnows to nominal concentrations of 10, 1, and 0.1 nM of E2 and discovered over a period of 19 days that exposure appeared to alter the timing of VTG production in females and VTG induction in males1.
Further physiological changes in fathead minnows exposed to varying levels of E2 were noted in a 1999 published study that showed a reduction in size of secondary sex characteristics (fatpads and nuptial breeding tubules) in males and a host of physiological reproductive changes in females, including an increase in atretic follicles2. In males, electron microscopy of seminiferous tubules and their Sertoli cells revealed large phagolysosomes filled with degenerative spermatozoa and other cellular debris2.
Industrial and Consumer Plastics Manufacturing
Besides the natural estrogen E2 and synthetic estrogen EE2, there exist a multitude of chemicals that are estrogenic in their effects on organisms. One such chemical is Bisphenol A (BPA), which is used in ubiquitous industrial and consumer plastics manufacturing throughout the world. One 2001 study investigated the reproductive effects of long-term exposure to BPA in the fathead minnow. Over the course of a multigenerational study spanning 164 days, researchers noted that BPA water concentrations as low as 640 mg/L half way into the study had significant effects on both male and female fathead minnows, including increased levels of VTG, arrested gonadal development in both sexes, and sex cell anomalies in the testis suggesting problems with spermatogenesis3. At levels of 1280 mg/L egg production was also affected, as was the rate of hatching in the following generation3. The study illustrated that the byproduct of the manufacture of such common household items as compact discs and plastic water bottles could significantly impact the health of aquatic organisms. However, the levels of BPA at which the subject fathead minnows were subjected are significantly higher than common exposure levels typically found in lakes, rivers, and streams.
'Anglish': Evidence exists suggesting industrial and consumer plastics manufacturing effluents may play a significant role in fish intersexing.
Cattle Feedlot Wastewater
In 2004 a group of researchers embarked in a new territory by investigating the effects of EDCs found in cattle feedlot wastewater on fathead minnows. What they observed in collected wild fathead minnows exposed to feedlot effluent (FLE) were several biomarkers not entirely dissimilar to those already noted in previous studies on the effects of E2, EE2, and BPA: 1) decreased testosterone synthesis; 2) arrested development of testicular development; 3) decreased estrogen-to-androgen ratio and subsequent defeminization of females4. Their hypothesis was that FLE containing animal hormone, pharmaceutical, and food byproducts comprised androgenic/estrogenic compounds that inhibited the release of gonadotropins4. This was the first study to suggest that FLE – like sewage treatment and industrial wastewaters – may have significant effects on fish reproductive and endocrine systems.
'Anglish': Cattle feedlot wastewater often contains animal hormone, pharmaceutical, and food byproduct hormones, all of which point to causing the same kind of fish intersexing observed with sewage treatment and industrial wastewaters.
Two years later a group of researchers from the Department of Fisheries, Wildlife, and Conservation Biology at the University of Minnesota published a paper discussing the role of environmental estrogens in suppressing hormones, behavior, and reproductive fitness in male fathead minnows. Operating from the premise that it is difficult to know the impact of sewage treatment plant effluent on wild fathead minnows and noting that previous researchers’ experiments had focused on larval fish development and the routine description of increased VTG and suppressed testosterone and KT, U of M researchers demonstrated how male competitive male reproductive fitness may be compromised as a result of environmental estrogen (EE) exposure by placing adult males with females in reproductive scenarios. Over the course of 5 days, fathead minnows were subjected to sewage treatment plant effluent (STPE), well water, E2, or methyltestosterone (MT) ( a cheaper alternative to KT). To simulate wild reproductive scenarios, researchers contrived a noncompetitive scenario of introducing one male into an aquaria with a nest and two females; and a second competitive scenario in which exposed males were introduced to an aquaria with two females, an unexposed male, and a nest.
The researchers observed: 1) STPE exposed males exhibited less agonistic behaviors, showed more sexual dimorphism, and had almost zero reproductive success when compared to control minnows; 2) E2 exposed males exhibited increased VTG production and compromised reproductive fitness (e.g. nest acquisition, egg fertilization, and young production) when in the presence of competing males; and, 3) MT exposed males exhibited more aggressive reproductive fitness than control males5. Unlike much previous work on the effects of estrogenic compounds on fathead minnows which focused almost solely on physiology, this study was one of the first to examine the effects that EEs have on behavior, illustrating that even short term exposure can bring about reproductive implications in competitive spawning scenarios.
'Anglish': University of Minnesota researchers discovered that not only do these estrogenic compounds change the reproductive physiology of fathead minnows, they also change reproductive behavior in an adverse way.
One of the most recently published studies in this area (March 2007) – conducted by researchers from Fisheries and Oceans Canada and the Molecular Indicators Research Branch of the EPA – determined that chronic exposure to EE2 led to feminization of male fathead minnows through production of vitellogenin (VTG) mRNA and protein, continued production of VTG in females beyond normal breeding season, impacts on gonadal development, as evidenced by intersex in males and altered oogenesis in females, and ultimately, near extinction of this species from the lake6. This exhaustive, 7-year whole-lake study demonstrated that chronic exposure can result in the complete loss of a species population.
'Anglish': Canadian researchers engaged in a 7-year study discovered that these compounds and the reproductive physiological/behaviorial changes that result can lead to a complete fish population collapse.
One of the major problems, especially with earlier studies, was the lack of sufficient protocols, procedures, and tests for most accurately determining the effects of estrogens on fathead minnows. A U.K. research team based at Brunel University published a paper in 2000 that sought to set a new precedent in EDC testing with fathead minnows by proposing shorter, partial life-cycle tests. The researchers contended that while there were a number of in vitro screening assays developed for endocrine mimics (including estrogens), none were fully adequate because: a) EDCs bioaccumulate and/or result from metabolism/environmental degradation of the parent compound; and, b) in order to show cause-effect relationships between exposure to EDCs and reproductive/physiological effect, it’s necessary to do whole animal studies7. Their proposed partial life-cycle test monitored reproductive performance in pair-breeding fathead minnows observed over two 3-week trials, one with exposure to 4-nonylphenol (4-NP) and one without. Although 4-NP is thought of as a weak estrogen mimic, its measured levels in wastewater effluents throughout the world are high enough to cause an hormonal imbalance in fish. Their study showed that high levels of 4-NP (>48 mg/L) were enough to shut off natural reproduction completely in the fathead minnow7. Later studies, like the U of M example, also filled in some of the gaps of earlier studies by not only working adult pair-breeding fathead minnows, but expanding the experiments to include a more comprehensive list of behaviors to monitor (e.g. agonistic behaviors, nest-directed behaviors) under the exposure of STPE, E2, and KT.
Sportfish In Question
One of the problems in all of the above studies is the lack of significant research and subsequent data illustrating the effects of EDCs – in this case estrogens – on fishes that live longer life spans. Short-lived fish species may generally be at the greatest risk from exposure to estrogens, but longer-lived species populations may be at similar risk with chronic exposure.
To date, there is only minimal research available on the effect of EDCs on larger freshwater teleost fish like brown trout, largemouth bass, walleye, northern pike, etc.
Inconclusive studies have pointed to similarly observed phenomena in the walleyes of Pool 2 of the Mississippi River in Minnesota but no one – at least as of yet – knows what influence estrogenic compounds have on walleye reproductive fitness behavior and subsequent population dynamics as a whole.
How might longer, low-level exposures manifest in reproductive physiology and behavior given EDCs bioaccumulate?
How might specific roaming populations of fishes avert the dangers of exposure?
How are river populations affected versus lake populations?
Likewise, given the reality of feedlot effluents, what effect do similar agricultural effluents have on trout, whose physiology and habitat is especially vulnerable?
These are but a few questions to ask ourselves as anglers and conservationists given what researchers have learned from the fathead minnow.
What have YOU experienced on your waters?
What have YOUR local environmental, academic and political organizations done to investigate this issue where YOU live?
I encourage you to find out, get involved and become a politcally-involved angler. Organizations like Trout Unlimited, American Sportfishing Association, Keep America Fishing, and your local rod and gun clubs are great places to get started.
Also, don't be scared to stop by your local natural resources or extensions office and get to know what they're studying in your area.
The future of our fisheries – and our sport – depends on it.
CONCLUSIONS
While the aforementioned studies do much to describe the physiological effects of exposure to estrogenic compounds, the real mystery of how these compounds affect reproductive behavior has largely been unanswered. Some researchers have touched on it, but there is still much more to explore.
What has been noted, however, is that regardless of the specific mechanisms at work, over time complete populations can implode due to chronic exposure to even moderate levels of estrogenic compounds.
In terms of risk assessment, these studies are the writing on wall.
The fathead minnow, as a sentinel, as an indicator species, as the canary in the coal mine, has provided a wealth of research in many scientific fields to help elucidate the questionable implications of waterborne EDCs.
While this blog (and my old research paper) has focused on estrogenic compounds, there are tens of thousands of chemicals currently in use in agriculture and industry, many of which have already proven their adverse effects on our environment8.
And, with the many advances in the industrial, military, and technological sectors, new types of chemicals are being introduced every day, which will demand risk assessment on various levels8. That said, I think the fathead minnow has some job security – both in our bait buckets and countless labs across the globe.
Again, I encourage you to learn more about the health of your local waters and the creatures that live there. Get involved; no one can protect the future of fishing better than a stalwart group of anglers who make their voices heard.
Slack is evi; tight lines,
Jim Edlund, NAFC online editor
Going forward, you can reach me at jim.edlund@gmail.com. I hope to hear from you – or better yet, run into you on the water! Happy trails!
Cited References
1. Giesey JP, Kramer VJ, Miles-Richardson S, Pierens SL. Reproductive impairment and induction of alkaline-labile phosphate, a biomarker of estrogen exposure, in fathead minnows (Pimephales promelas) exposed to waterborne 17b-estradiol. Aquatic Toxicology. 1998;40(4):335-360.
2. Barbee SJ, Fitzgerald SD, Giesy JP, Kramer VJ, Miles-Richardson SR, Render JA, Yamini B. Effects of waterborne exposure of 17b-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquatic Toxicology. 1999;47(2):129-145.
3. Caunter J, Evans M, Gargas M, Hetheridge M, Hurd K, Sohoni P, Sumpter JP, Toy R, Tyler CR, Williams T, Woods C. Reproductive effects of long-term exposure to Bisphenol A in the fathead minnow (Pimephals promelas). Environmental Science and Technology. 2001;35(14):2917-2925.
4. Binzcik GA, Gates JL, Gray LE, Guillette LJ, Horton MK, Kolok AS, Lambright CS, Orlando EF, Soto AM. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environmental Health Perspectives. 2004;112(3):353-358.
5. Hogarth W, Jones R, Martinovic D, Sorenson PW. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environmental Toxicology and Chemistry. 2006;26(2):114-121.
6. Blanchfield P, Evans R, Flick R, Kidd K, Lazorchak J, Mills K, Palace V. Collapse of a fish population after exposure to a synthetic estrogen. PNAS. 2007;104(21):8897-8901.
7. Harries JE, Harris CA, Hill E, Maddix S, Runnalis T, Sumpter P, Tyler CR. Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnows (Pimephales promelas). Environmental Science and Technology. 2000;34(14):3003-3011.
8. Ankley GT, Villeneuve DL. The fathead minnow in aquatic toxicology: Past, present and future. Aquatic Toxicology. 2006;78(1):91-102.
9. Ankley GT, Jensen KM, Kahl MD, Korte JJ, Pasha MS. Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2001;128(1):127-141.
10. Ankley GT, Jensen KM, Kahl MD, Korte JJ, Makynen EA. Description and evaluation of a short-term reproduction test with the fathead minnow. Environmental Toxicology and Chemistry. 2001;20(6):1276-1290.
11. Ankley GT, Jensen KM, Orlando EF, Watanabe KH. What is normal? A characterization of the values and variability in reproductive endpoints of the fathead minnow, Pimephales promelas. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2007; (146)3:348-356.