Male Wildlife Under Threat, Full Report

EFFECTS OF POLLUTANTS ON THE REPRODUCTIVE HEALTH
OF MALE VERTEBRATE WILDLIFE -

MALES UNDER THREAT
A CHEM Trust report by Gwynne Lyons

CHEM Trust’s aim is to protect humans and wildlife from harmful chemicals.
Based in the UK, it was set up in 2007 to take over the mantle of WWF-UK’s
work on toxic chemicals. CHEM Trust’s particular concerns relate to chemicals
with hormone disrupting properties, persistent chemicals that accumulate in
organisms, the cocktail effect and the detrimental role of chemical exposures
during development in the womb and in early life. CHEM Trust passionately
believes in the conservation of biodiversity and in the importance of wildlife
protection. Furthermore, monitoring wildlife populations can provide vital
insights into contaminant-related threats to human health, the protection of
which is of paramount importance.
Both wildlife and humans are at risk from pollutants in the environment.
CHEM Trust is working towards a time when chemicals play no part in causing
impaired reproduction, deformities, disease, deficits in brain function, or other
adverse health effects. Human exposure to some undesirable chemicals may
arise from contamination of the food chain and from the use and disposal of
many everyday products such as TVs, computers, cars, construction materials,
toys, toiletries and cosmetics.
CHEM Trust is committed to engaging with all parties, including regulatory

authorities, scientists and medical professionals to increase informed dialogue
on the harmful role of some chemicals. By so doing, CHEM Trust aims to secure
agreement on the need for better controls over certain chemicals, and thereby to
prevent disease and protect both humans and wildlife.
CHEM (Chemicals, Health and Environment Monitoring) Trust

gratefully acknowledges the support of the Esmée Fairbairn
Foundation.
Further copies of this report can be downloaded free from

www.chemtrust.org.uk
Cover photos clockwise from top left, include peregrine falcon [©iStockphoto.com-Mark Bond];
otter [Kindly provided by ©Hugh Jansman, Alterra]; Helsinki harbour [©iStockphoto.com-Dan Maso];
eland [©iStockphoto.com- Adrian Assalve]]; bald eagle [©iStockphoto.com-Frank Leung];
beluga whale [©iStockphoto.com-Klaas Lingbeek- van Kranen]; American robin [©Albert Steen-Hansen
Denmark]; Northern leopard frog [©iStockphoto.com-Steve Geer].
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EFFECTS OF POLLUTANTS ON THE REPRODUCTIVE HEALTH OF MALE VERTEBRATE WILDLIFE -
MALES UNDER THREAT
contents
Section 1: Summary and Overview.
Section 2: Pollutant-Related Effects Reported in Male Vertebrate Wildlife and

Effects on Reproduction.
2.1 Fish
2.2 Amphibians
2.3 Reptiles
2.4 Birds
2.5 Mammals
Section 3: Effects Reported in Wildlife in Polluted Environments, Endocrine

Disruptors and Mixture Effects.
3.1 Highly Contaminated Aquatic Environments
3.2 Endocrine Disruptors and Mixture Effects
3.3 Transgenerational Effects
Section 4: Conclusions and Recommendations.
Abbreviations and Technical Terms.
 BHC alpha benzene hexachloride (related to Lindane insecticide)

alternatively called alpha hexachlorocyclohexane.
anti-androgenic a hormone disruptor which works against the male hormone, androgen.
cryptorchidism undescended testes (bilateral refers to both testes, and uni-lateral cryptorchidism
means one testis is undescended).
EDCs endocrine or hormone disrupting chemicals. The term ‘endocrine disrupting
chemicals’ is interchangeable with the term ‘hormone disrupting chemicals’ or
‘hormone disruptors’. Hormone disruptors are substances, not naturally found
in the body, that interfere with the production, release, transport, metabolism,
binding, action or elimination of the body’s natural hormones, which function as
chemical messengers.
Dioxins polychlorinated dibenzodioxins (PCDDs), combustion products.
DDT dichloro diphenyl trichloroethane, an insecticide.
DDE dichloro diphenyl dichloroethylene, a contaminant or breakdown product of DDT
insecticide.
DNA deoxyribonucleic acid.
Furans polychlorinated dibenzofurans (PCDFs), combustion products.
HCB hexachlorobenzene, a fungicide.
OCs organochlorine chemicals.
Oestrogenic hormone disruptor mimicking the female hormone, oestrogen.
Ovo-testes eggs developing in the testes / intersex features.
PCBs polychlorinated biphenyls, a now banned persistent pollutant
which was used principally in electrical equipment.
TDS testicular dysgenesis syndrome.
TSH thyroid stimulating hormone.
VTG vitellogenin, the egg yolk precursor protein made by females.
ii
MALES UNDER THREAT
section 1
summary and
overview This paper provides a review of the All vertebrates have similar sex
reported effects on the reproductive hormone receptors, which have been
health of male vertebrate wildlife, conserved in evolution. Therefore,
which are known or suspected to be observations in one vertebrate wildlife
associated with pollutants. Males species, may serve to highlight
of species from each of the main pollution issues of concern for other
classes of animals in the vertebrate vertebrates, including humans.
sub-phylum (including bony fish, Indeed, given the widespread
amphibians, reptiles, birds, and presence of endocrine disrupting
mammals) have been affected by chemicals in the environment,
chemicals in the environment, effects are likely to be occurring in
particularly chemicals with hormone more species than those currently
disrupting properties. Man made reported. Endocrine disrupting
chemicals that can disrupt the male chemicals (EDCs) de-rail the body’s
and/or female sex hormone may chemical messenger system, the
adversely affect the ability of an hormones, and therefore this term is
organism to reproduce, although used interchangeably with the term
chemicals which affect reproduction ‘hormone disruptors’. Auxiliary
by other mechanisms are also of signalling chemicals such as enzymes,
concern. growth factors, and so forth, may also
be disrupted. There is much “cross
talk” in the body, and, for example,
pollutant related disruption of brain
neurochemistry can be an early step
in reproductive impairment (Basu and
Head,2008). The mounting concern
is such that between 1998 -2007 the
European Commission invested 161
million Euros into research into the
phenomenon of endocrine disruption.
Section 2 summarises the effects

reported in male vertebrate wildlife.
These include altered hormone levels,
reduced number of sperm, genital
deformities and deformities of other
structures under sex hormonal
influence. Many of these reported
effects are known or suggested to
be due to exposure to EDCs in the
environment. Feminization of the
males of numerous vertebrate species
is now a widespread occurrence, with
many males of egg laying vertebrate
found to be abnormally producing
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MALES UNDER THREAT
the egg yolk precursor protein, reproductive tract; embryonic Section 3 provides an overview
vitellogenin. Vitellogenin (VTG) mortality; reduced reproductive of some of the findings in wildlife
is synthesized by the liver of non- success including egg-shell thinning; living in polluted environments. This
mammalian vertebrates and induced and poor parenting behaviour. section also highlights the difficulties
in response to oestrogen. A decrease of identifying which particular
in male sex hormone, or in the ratio Effects in the males of numerous pollutants are to blame for such
of the male:female sex hormones mammalian species have been effects, and summarises the concern
can lead to weak male secondary sex reported, and include the following. about effects due to simultaneous
characteristics including intersex In rodents: reduced sperm; exposure to more than one chemical,
reproductive organs (part female reduced testes weight; and reduced the so called ‘mixture effect’. Several
ovary, part male testis), small penis, reproduction. oestrogenic and anti-androgenic
ineffective mating behaviour, and In otters and/or mink: reduced chemicals that have been found in
possibly low fertility. This review baculum (penile bone) length; smaller polluted rivers and lakes are noted, as
also highlights some species where testes; and impaired reproduction. is the anti-androgenic activity found
reduced reproduction has been In seals and/or sea lions: in discharges from UK sewage works.
noted, but this may be due to effects impaired reproduction (including Furthermore, this section highlights
of contaminants on the female of implantation failure, sterility, that concern for the long-term health
the species, rather than the male. abortion, premature pupping). of wildlife populations and humans is
Moreover, the mechanisms of action In cetaceans: reduced testosterone enhanced because several laboratory
by which some of the effects occur are levels; impaired reproduction; and studies have suggested that disorders,
not known with certainty. hermaphrodite organs. such as deficits in sperm production,
In polar bears: intersex features can be passed on to subsequent
In male vertebrate wildlife the and deformed genitals; reduced testes generations, who themselves have not
following effects, which are known or and baculum length; low testosterone been exposed. Such effects are termed
suspected to be caused by pollutants, levels in adult males; and reduced cub transgenerational.
have been reported. survival.
In black bears: undescended testes.
In fish: abnormal secretion in males In Florida panther: abnormal
of VTG; altered spermatogenesis; sperm and low sperm density; Section 4 draws conclusions and
eggs developing in testes (ovo-testes/ undescended testes; and altered recommendations. It underlines the
intersex); intersex genital apparatus; hormone levels. similarities of the reported effects in
and poor reproductive success. In deer: antler deformities; male vertebrate wildlife, and therefore
undescended testes; and testicular notes the concern for human male
In amphibians: abnormal abnormalities, including cells reproduction. Conclusions are also
production of VTG by males and ovo- predictive of testicular cancer. reached regarding the need for tighter
testes/intersex features. In eland (an antelope): regulation of EDCs in order to reduce
abnormal testes, including impaired exposures. In addition, the need for
In reptiles: abnormal production spermatogenesis. ongoing monitoring of wildlife is also
of VTG by males: sex hormone highlighted, as is the need for more
disruption; ovo-testes; smaller phallus These findings are tabulated in research to understand the long-term
in alligators and shorter estimated Table 1, and are discussed in more implications of chemical exposures for
penis length in turtles; decreased detail in Section 2. Taken together, life on earth.
hatching; and decreased post hatch it can be seen that feminisation
survival. or de-masculinisation of males is
widespread.
In birds: abnormal VTG production
in male birds; deformities of the
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MALES UNDER THREAT
section 1
summary and
overview
(cont)
Table 1: Effects reported in wildlife which are known or suggested to be linked to chemical contaminants
Reduced Intersex / Deformities VTG Other Sex

reproduction Abnormal of sex linked in male linked effect
Testes structure /
reduced
phallus/
baculum
FISH Fish Y Y Y Y
AMPHIBIAN Frogs/Toads Y Y Y Reduced no.
of nuptial
pads in males
REPTILE Alligator Y Y Y
Turtle Y Y Y Y
BIRDS BIRDS Y Y Y Egg
shell
thinning
MAMMALS Rodent Y Y
Otter Y Y Y
Mink Y Y
Seal / Sea Lion Y
Whales Y Y
(Cetaceans)
Polar Bears Y Y Y
Black/Brown Y
Bears
Panther Y Y
Deer Y Y Deformed
antlers in
males
Eland Y
Y = Effect reported and known or suggested to be linked to contaminants
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MALES UNDER THREAT
section 2
pollutant-
related effects
reported in
male vertebrate
wildlife and
effects on
reproduction Many wildlife species are now Field studies of wildlife are expensive
reported to be affected by pollutants, and time consuming to conduct
and similarities can be seen in and there is therefore a paucity of
the effects recorded. The target information on most species. Apart
sites which are the focus of this from studies in highly polluted areas,
review include male developmental most of the data on wildlife come from
pathways. It is clear that structural species hunted for food, particularly
intersex features, including effects fish.
on the male reproductive tract, result
from exposure before birth. On the Table 1 illustrates that defects linked
other hand, abnormal secretion of to male reproductive development
the egg yolk precursor protein, VTG, appear to be common to wildlife
in male fish, birds, and reptiles, can species from each of the classes
result from later adult-life exposure of animals that make up the
to feminising pollutants. VTG is vertebrate sub phylum. It shows
normally produced in females, and that contaminants are affecting
when found in males in elevated the reproductive health of males
concentrations it confirms the of many species. Feminisation
presence of sex hormone disrupting or de-masculinisation of males is
contaminants in the environment, widespread.
and indicates feminisation of the
male. Reduced reproduction has also
been included, although it may result
from female or male reproductive
impairment, or from lack of viability
of the offspring.
4
MALES UNDER THREAT
2.1
fish Fish may be particularly affected by In fish, the following effects have
pollutants, because their exposure been particularly noted: abnormal
is not only via the diet, but also via secretion of VTG in males; altered
the gills and skin. The physical spermatogenesis; eggs developing
chemical characteristics of many in testes (ovo-testes/intersex);
EDCs, especially their lipophilicity intersex genital apparatus; and poor
(“fat-loving” properties) also favour reproductive success.
their movement from the surrounding
water into biological tissues. VTG, the precursor of the egg yolk
protein, is normally not detectable
in male fish, or is only present at
very low levels. Therefore, detection
of elevated levels in male fish is
abnormal, and is an excellent
biomarker of exposure to oestrogenic
EDCs. Furthermore, VTG induction
is generally accompanied by various
degrees of reproductive interference
at similar or lower ambient oestrogen
concentrations. This means that
it can be a marker for a number
of adverse effects (for review see
Matthiessen,2003)
If reproduction in males is
compromised, and fewer males
contribute to the next generation,
this would not necessarily affect
the population in the short term.
Population levels may largely depend
on the number of female offspring
that result from the average female’s
lifetime reproductive activity
(Gurney,2006). Nevertheless, a
considerable proportion of breeding
males are believed to be necessary
in order to sustain a genetically
viable population in the long term
(IEH,2004). The following examples
represent some of the studies showing
a link between exposure to EDCs and
effects in fish from the Osteichthyes
class (the bony fish).
5
MALES UNDER THREAT
Abnormal Production of
Vitellogenin (VTG) in Male Fish
Studies in UK freshwaters were the reported in many species and many
first to report the phenomenon of countries worldwide, including:
VTG production in male fish (Purdom cod (Gadus morhua) from the
et al.,1994; Harries et al.,1996). North Sea (Scott et al.,2006); dab
Similarly, subsequent UK studies (Limanda limanda) from the North
by Lye and co-workers (1997;1998) Sea, Irish Sea and English Channel
were the first to report VTG induction (Scott et al.,2007); flounder from
and testicular abnormalities in a UK estuaries (Platichthys flesus)
marine fish, the flounder (Platichthys (Kirby et al.,2004); flounder from
flesus). In many UK fresh waters Denmark; flounder from a Dutch
downstream of sewage treatment harbour and a Dutch offshore
works it seems that a large part of spawning ground; sole (Pleuronectes
the oestrogenic component is derived yokohamae) from Japan; grey
from the natural female hormones mullet (Mugil cephalus) from Osaka
(oestrone and oestradiol-17) and the Bay in Japan; sole (Parophrys
contraceptive pill (ethinyl oestradiol) vetulus) from Puget Sound, USA (for
excreted in sewage (Jobling and review see Matthiessen,2003); and
Tyler,2003). However, in some UK Mediterranean swordfish (Xiphias
rivers, industrial chemicals, such gladius) from the Straits of Messina Flounder - normal testis tissue seen through
microscope.
as nonylphenol, have also been near Sicily, where VTG induction
[Photo kindly provided by ©Mark Kirby,
implicated as a causal factor in VTG was seen at very high levels (Fossi et CEFAS Lowestoft]
production (Thorpe et al.,2001; al.,2004).
Lye et al.,1999). Similarly, in the
Mediterranean, some researchers
suggest that oestrogen mimicking
organochlorine contaminants may
play a role (Fossi et al.,2004).
VTG production in several wild male

freshwater fish species has now been
reported in many places worldwide
including Europe, North America,
Flounder - Ovotestis. The circles are eggs in
Australia, Japan and Africa. In Male flounder and other marine fish, includng the testis. Up to a fifth of male flounder from
cod, dab, sole, grey mullet and swordfish certain sites in some UK estuaries are intersex.
the Republic of Benin in Africa,
have been found to be abnormally making the [Photo kindly provided by ©Mark Kirby,
for example, VTG in male tilapia female egg yolk protein CEFAS Lowestoft]
(Sarotherodon melanotheron) has
been associated with organochlorine
pesticide contamination in the Ouémé
River (Okoumassoun et al.,2002).
Similarly, VTG production in male
marine fish has also now been
6
MALES UNDER THREAT
2.1
fish Intersex in Fish
(cont) The presence of intersex or ovo-testis upstream, or the fact that breeding
(ie. primary or secondary oocytes grounds for marine species are further
(eggs) abnormally present in the offshore and therefore probably
testicular tissue of the male) is now less contaminated. Nevertheless,
a frequently reported phenomenon in some very oestrogenically
in fish. This disrupted gonad contaminated UK estuaries
development is almost certainly (Mersey, Tyne, Clyde and Forth)
linked to endocrine disruption caused up to a fifth of the male flounder
by exposure to hormone disrupting and blenny (eelpout) (Zoarces
compounds. It can be induced viviparous) in some locations show
experimentally through exposure at ovo-testes, whereas ovo-testes has
the larval stage, but not by exposure of not been seen in flounder from a
the adult fish. Male fish with intersex relatively uncontaminated reference
organs typically produce fewer motile estuary, the Alde (for review see
sperm than those with normal testes. Matthiessen,2003).
Intersex has been reported to varying
degrees, in (up to 100% of) freshwater Intersex is now known to be
roach (Rutilis rutilus) at some widespread. For example, apart from
locations on UK rivers (Jobling and in the UK, it has been reported in
Tyler,2003). fish from the Seine estuary in France
(flounder); the southern Baltic in
Freshwater fish species in which Germany (flounder);Tokyo (flounder);
abnormal intersex has been the Mediterranean (swordfish)
reported include: roach; bream (for review see Matthiessen,2003);
(Abramis abramis); chub (Leuciscus South Africa (sharptooth catfish)
cephalus); gudgeon (Gobio gobio); (Barnhoorn et al.,2004); the Potomac
barbel (Barbus plebejus); perch river (small mouth bass) (Blazer et
(Perca fluviatilis); white perch al.,2007); the St Lawrence river in
(Morone Americana) (Kavanagh et Quebec (lake whitefish) (Michaelian
al.,2004); stickleback (Gasterosteus et al.,2002); and in a polluted area
aculeatus); shovel-nosed sturgeon of Lake Ontario, where 83% of male
(Scaphirhynchus platyorynchus) white perch collected in 1999-2000
(for review see Jobling and had intersex features, which was
Tyler,2003); sharptooth catfish an increase on the previous year
(Clarias gariepinus) (Barnhoorn et (Kavanagh et al.,2004).
al.,2004); lake whitefish (Coregonus
clupeaformis) (Michaelian et
al.,2002) and smallmouth bass
(Micropterus dolomieu) (Blazer et Deformities of Sex-Linked
al.,2007). Structures in Fish
There are species differences in the
The phenomenon of intersex in response of fish to exposure to sex
estuarine and marine fish in the hormone disruptors. For example,
UK appears to be less than in some sand gobies (Pomatoschistus minutus
UK freshwater fish, but it is not and P.lozanoi) from contaminated
known whether this is due to species estuaries in the UK do not show either
differences in response, higher induction of VTG or intersex, but
exposures in the freshwater instead male fish exhibit deformed
7
MALES UNDER THREAT
and feminised urogenital papillae, not identified, some of the minor p-nonylphenol, diethylphthalate,
which is the structure used by both contributors to the oestrogenic or dimethylphthalate, dibutylphthalate
sexes to deposit gametes (Matthiessen feminising activity were reported and DEHP (Bornman et al.,2007).
et al.,2002). In males, the papillae to be nonylphenol, cinnarizine (an
can be considered equivalent anti-histamine drug), and cholesa-
to the penis. This phenomenon 4,6-dien-3-one (a natural cholesterol
in sand gobies has been termed degradation product) (Allen et Poor Reproductive Success /
morphologically intermediate papilla al.,2002).
Reduced Hatching in Fish
syndrome (MIPS), and was found
In Lake Ontario, contaminants
in males from the UK Tees, Mersey Structural defects of the reproductive
were considered responsible for
and Clyde estuaries. This feminised apparatus have also been noted in
the loss of lake trout (Salvelinus
condition was found in areas of known other fish species. In Florida USA,
namaycush) in the 1960s (Cook et
oestrogenic contamination, and mosquito fish (Gambusia holbrooki)
al.,2003). Moreover, even after the
laboratory experiments provided good from the pesticide polluted Lake
extinction of this population of lake
evidence that it is probably caused by Apopka were compared with those
exposure to environmental endocrine from less polluted lakes. Male fish trout, and re-stocking, there was a
disruptors. Nevertheless, in the wild from the polluted Lake Apopka had lack of reproductive success, with
the precise causal agent(s) were not slightly shorter gonopodia and fewer reduced fry survival still occurring
identified. sperm cells per milligram weight after 1980 (Cook et al.,2003). Cook
of testis, when compared with the and colleagues took sediment
fish collected from Orange Lake and cores and were able to show that
Lake Woodruff. The growth and lake concentrations of dioxins and
development of the modified anal dioxin-like chemicals were probably
fin (the gonopodium) is a secondary to blame, because at the time of the
Sand Goby
sexual characteristic in males under crash, and for some years afterwards,
the influence of testosterone, and these were sufficient to affect the
is critical for sperm transfer. The breeding of these top predator fish.
authors concluded that sexual
characteristics of relevance to male Reduced spawning success or
reproductive capacity are altered reduced hatching has been noted
Sand goby Sand goby - Male sand in the Lake Apopka mosquitofish in several wild populations of
- normal normal male goby with population, and that anti-androgenic
female papilla, papilla (penis) feminsed or marine fish, including: a DDT
seen through intermediate chemicals were a possible cause of the
contaminated population of white
microscope. (MIPS) effects (Toft et al.,2003). Similarly,
papillae. croaker (Genyonemus lineatus)
effects on the gonopodia of male
[All 3 photos kindly provided by ©Mark Kirby, in California; a variety of flatfish
CEFAS Lowestoft] mosquitofish taken from polluted
species (P.bilineatus and P.vetulus)
wetlands in Western Australia have
in the Puget Sound, USA; PCB
In some UK estuaries and effluents, been noted (Game et al.,2006).
contaminated Baltic flounder;
substances present with reported In South Africa, abnormalities of the
oestrogenic activity included PCB or DDE contaminated Baltic
sexual papillae were found in male
the natural steroids, particularly sharptooth catfish from a nature herring (Clupea harengus); and
17-oestradiol, and some synthetic reserve in Pretoria. At four sampling organochlorine contaminated Baltic
man-made compounds, including sites in the reserve and in various cod (Gadus morhua) (for review see
nonylphenol and di-(2-ethylhexyl) matrices, several chemicals were Matthiessen,2003).
phthalate (DEHP). In sediments, present. These included residues of
much higher oestrogenic activity was -BHC, lindane, endrin, heptachlor
identified, and although the main epoxide, methoxychlor, DDT and
contributors to this activity were metabolites, and octylphenol,
8
MALES UNDER THREAT
2.2
amphibians Many amphibian species worldwide Reproductive System Defects,
are in decline, with an estimated one VTG Production and Intersex in
third now either threatened or extinct Amphibians
(IUCN,2008a). Habitat degradation Intersex features, linked to chemical
is suggested to be the main exposure, have been seen in the
contributory factor, but pollution may wild in both frogs and toads, and
also play a role. Indeed, pesticides and feminisation of males may lead to less
industrial chemicals can be carried reproductive success.
to remote areas far from the site of
their release. In California’s snow- Hayes and co-workers observed
capped Sierra Nevada, populations retarded gonadal development
of frogs and toads have crashed, (gonadal dysgenesis) and oocytes in
including the yellow-legged frogs the testes of wild leopard frogs (Rana
(Rana boylii and Rana muscosa) pipiens) collected from atrazine-
and the California red-legged frog contaminated sites across the USA
(Rana aurora), with some researchers (Hayes et al.,2003). They suggested
suggesting that the high levels of that atrazine could be causing these
pesticides transported in the air are effects in wild amphibian populations,
responsible (Sparling et al.,2001). and showed that atrazine exposure
In male amphibians abnormal in the laboratory (at 0.1ppb) resulted
production of VTG and intersex in intersex characteristics in leopard
features have been noted in some frogs. In male leopard frogs exposed
polluted locations. It is therefore in the laboratory to 0.1ppb of atrazine,
speculated that some of the decline testicular oocytes were found in 29%
in amphibians may be due to effects of the males, and in some cases the
on reproduction, although studies oocytes were vitellogenic (Hayes,
also suggest immune suppression 2004). Furthermore, Hayes and
due to chemical exposures may be a colleagues (2003) have hypothesised
Northern leopard frogs in the wild have been factor (Linzey et al.,2003; Christin et that atrazine might induce aromatase,
found with eggs in the testes. al.,2004; Fenoglio et al.,2005; Hayes which converts testosterone to
[©iStockphoto.com-Steve Geer]
et al.,2006). oestrogen, thereby increasing
the production of endogenous
oestrogen. However, another team
of researchers have reported that
higher concentrations of atrazine are
needed to cause such effects (Carr et
al.,2003). These workers subsequently
concluded, after conducting outdoor
experiments in tanks, that oocytes in
the testes of the African clawed frog
(Xenopus laevis) may be a natural
phenomenon (Jooste et al.,2005).
However, several other amphibian
experts have expressed doubts about
this latter finding (Renner,2005)
and it may be a temperature related
effect or perhaps due to other EDCs
contaminating the water in the tanks.
9
MALES UNDER THREAT
In a study in Illinois, Reeder and testes and ovarian tissue present, Steroid hormone concentrations and
co-workers (1998; 2005) concluded female colouration called mottling, secondary sexual traits correlate with
that several chemical contaminants reduced nuptial pad number and reproductive activity and success, and
including PAHs, PCBs, dioxins, smaller forearm widths. In the most the authors therefore maintain that
furans, DDT and possibly atrazine, heavily farmed areas almost 40% of the affected toads are likely to have
were likely to have contributed to the male toads were intersex, and had reduced reproductive success, and
the decline of cricket frogs (Acris both testes and ovarian tissue. that these reproductive abnormalities
crepitans). From studying museum might certainly contribute to
collections they considered that the Testosterone levels were also lower in amphibian population declines in
proportion of intersex individuals the toads living in agricultural areas areas with agricultural contaminants
peaked during the period 1946 -1959. compared to those in cane toads from (McCoy et al.,2008).
The genetic sex of these frogs was not more suburban areas. Oestradiol
confirmed, but it was believed that levels were not affected, but due to the
the ones with ovo-testes were males reduction in testosterone, the intersex
(Beasley,2008). toads from the agricultural areas also Other abnormalities and altered
hormone levels in amphibians
A disorder characterised by an
extra or malformed limb(s) has
been reported in frogs, with some
scientists suggesting that this may
be linked to chemicals, UV exposure,
trematode infection, acid rain,
viruses, nitrates, or a combination of
these (Kiesecker,2002; Gardiner et
al.,2003; Ankley et al.,2004; Bridges
et al.,2004).
A USA survey of bullfrogs (Rana

catesbeiana) and green frogs (Rana
Male cane toads with intersex testes and lower testosterone have been found in Florida where
pesticides, including atrazine and glyphosate, are used. [©iStockphoto.com-Eric Delmar] clamitans) in New Hampshire, USA,
showed malformed frogs at 81% of the
Male cane toads (Bufo marinus) had a higher ratio of oestrogen to sites sampled (13 of 16 sites). Brain
in the wild are also exhibiting testosterone (McCoy et al.,2008). gonadotropin-releasing hormone, and
signs of feminisation. McCoy and androgen and oestradiol synthesis,
colleagues (2008) have studied Accumulation of the female egg yolk hormones essential to reproductive
populations in sugar cane fields precursor protein, VTG, was seen in processes, were measured in
in the Florida Everglades where the Bidder’s organ of around 20% tissues taken from malformed and
pesticides, including glyphosate and of the male toads from agricultural normal frogs. Significantly lower
atrazine, are used. These toads were areas. This is only known to occur concentrations (nearly 3-times less)
compared with toads living in areas after castration, and it is therefore of (in-vitro produced) androgens
with less agriculture. The number considered that the testes are and of brain gonadotropin releasing
and severity of feminised toads was necessary to suppress accumulation of hormone were found in malformed
greatest at sites with more agriculture, VTG in the Bidder’s organ. Therefore, compared to normal frogs. The
and the number of abnormalities the authors concluded that their researchers suggested that
and frequency of intersex gonads findings suggested that the testes of environmental factors or endocrine-
increased with agriculture in an the affected toads were disrupting chemicals that cause
application-dependent fashion. malfunctioning. Indeed, all the developmental abnormalities may
reported effects were considered also be responsible for these reduced
Effects reported in the males, included suggestive of compromised testicular hormone levels (Sower et al.,2000).
intersex characteristics with both function.
10
MALES UNDER THREAT
2.3
reptiles Studies of long-lived species like Turtles
turtles and alligators can provide a
very useful indicator of the health of At a heavily polluted site on the Great
wetland ecosystems. In the reptile Lakes in 2001, around 10% of the
class, turtles and alligators have been adult male snapping turtles (Chelydra
the subject of numerous studies. In serpentina) were found to be
turtles, the following effects have abnormally producing VTG, indicating
been noted: abnormal production sex hormone disruption (EC,2003).
of VTG by males; deformities of the
reproductive tract (including ovo- Furthermore, studies in snapping
testes and shorter estimated penis turtles from the Great Lakes and the
length); and decreased hatching/ St Lawrence River in Canada have
reproduction. In alligators, the found differences in the physiology
effects include: sex hormone of adult turtles taken from highly
disruption; smaller phallus; testicular contaminated sites compared to
abnormalities; reduced clutch viability those from less contaminated sites.
resulting from fertilisation failure At all sites, the precloacal length
and embryo mortality; and decreased of male hatchlings was larger than
post-hatch survival. that of females by an equal amount
at any given body size. However,
the precloacal length of both males
and females from the polluted site
increased with body size at a slower
rate than males and females from
the cleaner sites. These alterations
in secondary sexual characteristics
are believed to be initiated early
in development, are linked to
contaminant levels, and may result
in permanent organizational changes
in morphology (de Solla et al.,2002).
Precloacal length is also used as an
estimator of penis length, and in a
2001 study, this was shorter in male
adult turtles from the Detroit River,
and in juvenile males from two
polluted sites, as compared to cleaner
reference sites (EC,2003)
Male snapping turtles from polluted sites in the

Great Lakes are abnormally making egg yolk
protein, and appear to have smaller penises.
[Photo from Nova Scotia Museum of Natural
History Website]
11
MALES UNDER THREAT
Decreased hatching success has also Alligators

been reported in snapping turtles in
polluted sites around the Great Lakes Guillette and others have reported
compared to those from reference population decline and numerous
sites (EC,2003). At a particularly reproductive abnormalities in
polluted site, there were no signs alligators (Alligator mississippiensis)
of reproductive activity in the adult from Lake Apopka in Florida.
snapping turtles (EC,2003). There
is also a suspicion that deformities
in Great Lakes hatchlings, which are
found at higher rates than in cleaner
reference locations, may be linked to
chemicals.
Turtles living in polluted sites

Professor Lou Guillette carefully examining
elsewhere are also affected. For
alligator eggs. Lou’s work has been pivotal in
example, in Lake Apopka in Florida, unravelling the effects of pollutants in reptiles.
which is contaminated with several
EDCs, many new-born red belly This is a lake which is reported to be
Male alligators in polluted waters have been
turtles (Pseudemys nelsoni) have polluted with several organochlorine found with smaller phalluses and abnormal
been reported with genital disruption. pesticides, including dicofol and DDT testes. [©David Southern]
Here, abnormal testes, including chemicals, following a spill in the

ovo-testes were found (Guillette 1980s. However, effects have also High embryo mortality in alligators
et al.,1995). Also for example, been noted in alligators from Florida and high exposure to organochlorine
male yellow-blotched map turtles lakes polluted by diffuse sources. pesticides has been found in Florida
(Graptemys flavimaculata) from The following reproduction-related in Lakes Apopka and Griffin, and
a polluted Mississippi site exhibit abnormalities in Florida alligators Emeralda Marsh, as compared to
reduced reproduction, and some have been suggested to be linked less polluted sites at Lakes Woodruff
males were found to have high levels to exposure to EDCs: sex hormone and Orange (Sepulveda,2004).
of oestradiol (equivalent to levels disruption (including large adult Research has shown that low rates
found in females) and significantly males with higher oestrogen and of hatching were due to fertilization
lower testosterone (Shelby and lower testosterone levels than normal failure as well as early embryonic
Mendonça,2001). males of the same age); smaller mortality (SBRP,2003). Furthermore,
phallus (penis) in males; abnormal recent work by Lou Guillette’s team
testes; and reduced clutch viability has reported increased post-hatch
resulting from fertilisation failure mortality, as well as loss of sexually
and embryo mortality (Woodward et dimorphic gene expression in
al.,1993; Guillette et al.,1994; 1995; alligators from the contaminated Lake
2000; Guillette and Iguchi,2003). Apopka (Milnes et al.,2008).
Male red-belly turtles in Lake Apopka in Florida

have been found with eggs in their testes.
[Photo kindly provided by Tom Coy, Austin’s
Turtle Page]
12
MALES UNDER THREAT
2.4
birds In birds, oestrogen is the For birds to be exposed to pollutants
differentiating hormone for both during the critical period of
gonads, and for behaviour (see Giesy development, compounds must be
et al.,2003). This is in contrast to passed from the female bird to her
sexual differentiation in mammals, eggs. DDT is known to be readily
where it is androgen that causes the transferred to the lipid-rich yolk,
testes to develop, such that in the but it seems that several other
absence of androgen, the female is the contaminants, including large
default sex. In birds, in the absence molecules like deca brominated
of oestrogen, both gonads develop diphenylether (deca-BDE) can also
into testes, whereas during normal be transferred into the egg (see EU
female development, the left gonad RAR). Fish eating birds may be
develops into an ovary while the right particularly exposed to persistent and
gonad regresses (Fry,1995). Such bioaccumulating contaminants.
differences in the control of early life
developmental processes may mean In birds, pollutant related effects
that birds respond to environmental include: abnormal VTG production
endocrine disruptors rather uniquely. in male birds; deformities of the
reproductive tract; embryonic
mortality; reduced reproductive
success including egg-shell thinning;
and poor parenting behaviour.
Abnormal VTG Production in

Male Birds
In 2001, male herring gulls (Larus
argentatus) from a polluted area
around the Great Lakes were
found with elevated levels of VTG
in their blood. As in fish, this egg
yolk precursor protein is normally
produced by breeding females
(EC,2003). Therefore, this indicates
that these male birds were being
feminized. A team working in
Guadalajara in Spain has also found
raised VTG levels in male peregrine
falcon (Falco peregrinus), suggesting
a potential ongoing threat to birds of
prey. The peregrine falcon in Spain
is considered vulnerable, and in this
population over the last decade,
Male peregrine falcon in Spain have been feminised, and are abnormally making the female egg yolk a decrease in successful breeding
protein. pairs has been reported (Jiménez et
[©iStockphoto.com-Mark Bond]
al.,2007).
13
MALES UNDER THREAT
Deformities of the Reproductive

Tract and Ovo-testes in Male
Birds
There appear to be few studies of the
internal reproductive tract in birds.
However, in 2001, a male herring
gull (Larus argentatus), nesting in
the lower Great Lakes (downstream
of a polluted area) was found with a
significantly feminized reproductive
tract (EC,2003).
Szczys and colleagues (2001) noted

that at Bird Island, off the coast
of Massachusetts, the sex ratio
of hatched roseate tern (Sterna
dougallii) chicks was biased (55%) in
favour of females, raising concerns
about the male of the species. These
observations of skewed sex ratios
and female-female pairing among
endangered roseate terns gave rise
to investigations in common terns
(Sterna hirundo), as a surrogate
tern breeding in Massachusetts. In
1993/94, 60-90% of hatching male
common tern embryos sampled
exhibited ovarian cortical tissue in
their testes (ovo-testes). However,
examination of 21 day old common
terns collected from Bird Island in
1995, suggested that the ovo-testes
may become fully regressed and
therefore do not lead to permanent
alterations in gonadal tissue that
would be expected to impair
reproduction. It has also been
speculated that ovo-testes might occur
naturally in some common terns at
hatching, although the frequency with
which it occurs might be enhanced
Male herring gulls around the Great Lakes have been feminised by pollutants. by exposure to contaminants (Hart et
[©iStockphoto.com-Richard Thornton]
al.,2003).
14
MALES UNDER THREAT
2.4
birds Embryonic Mortality and Numbers of bald eagles (Haliaeetus
(cont)
Reduced Reproductive Success leucocephalus) are recovering slowly
in Birds in North America. However, those
Early concerns about the effects of nesting near the Great Lakes have
pollutants in birds stemmed from greater difficulty reproducing than
reproductive and developmental those nesting elsewhere, presumably
effects that were reported in the Great because their food supply remains
Lakes, particularly in fish eating contaminated. Furthermore, more
birds. One notable phenomenon was than half the bald eagles that do
female-female pairing in herring gulls. manage to hatch along the shores of
DDE was found to cause abnormal the Great Lakes, die young (EC,2001).
development of male birds exposed in
the egg, and therefore it was suggested Reduced reproduction has also
this might have caused a reduction in been noted in eagles in the Arctic.
the number of normal males returning For example, bald eagles had less
to the breeding colony. In the early offspring on Kiska Island, and this
1970s in Lake Ontario, where DDE was associated with raised levels of
levels were high, nests with five or DDE and organochlorine pesticides
more eggs (supranormal clutches) (AMAP,2004). Furthermore,
were seen as a result of two or more organochlorine levels in some
females occupying the same nest. other species of predator birds are
Supranormal clutches were still being considered to exceed those associated
found 25 years later, and very few of with effects on reproduction
these eggs were fertile (see EC,1997). (AMAP,2004; Knudsen et al.,2007).
In surveys during 2001-2004,
reduced embryo viability was still
seen in herring gull eggs, although the
precise cause of this was not known
(Fox,2005).
Bald eagles around the Great Lakes and in the Arctic are not reproducing well.
[©iStockphoto.com-Frank Leung]
15
MALES UNDER THREAT
More recently, pollutant-related eight persistent organohalogen

effects on reproduction, suggested contaminant classes (i.e. major
to be mediated through disruption organochlorines and brominated
of reproductive steroid or thyroid flame retardants and associated
hormones, have been reported in metabolic products) in the blood
glaucous gulls (Larus hyperboreus) of wild glaucous gulls in the Arctic.
breeding in the Arctic. These include They suggested that organohalogen
altered reproductive behaviour such contaminants may alter prolactin
as lower nest-site attendance in secretion in male glaucous gull and
males and reduced ability of males to may be a contributing factor to the
maintain the temperature of the nest adverse effects observed on the
while incubating (Bustnes et al.,2001; reproductive behaviour, development
2003; Verboven et al.,2008a). and population size of these gulls
breeding in the Norwegian Arctic.
Tree swallows nesting along the polluted Hud-
son river in the USA have been found to build Another study of glaucous gulls in
small, low quality nests. Svalbard suggested that there were Despite the generally lower levels of
[Photo kindly provided by John Peterson
contaminant-induced changes in organochlorine contaminants (OCs) in
Myers]
the sex hormone levels in the eggs of Antarctic biota, some compounds may
There are several reports of altered glaucous gulls, and it was speculated exceed the levels in equivalent Arctic
parenting behaviour in birds leading that these could affect offspring species. In 65 nests of south polar
to reduced reproductive success, performance over and above the toxic skuas (Catharacta maccormicki),
although there is not an abundance effects brought about by the persitent both males and females were caught,
of research in this area. For example, pollutants in the eggs (Verboven et and it was found that although the
reproductive failure of a number of al.,2008b). concentrations of organochlorines
fish-eating birds was observed around were below those documented to have
the Great Lakes in the mid-1960s reproductive effects in other aquatic
to mid-1970s, and investigations in birds, the eggs of females with the
the herring gull (Larus argentatus) higher levels of organochlorines in
showed that this was due to decreased their blood hatched later, and their
nest attentiveness during incubation, chicks were in poorer condition
and to direct embryotoxic effects at hatching than those of females
(Peakall and Fox,1987). Similarly, with lower levels. Thus, these
in Forster’s Tern (Sterna forsteri) organochlorine contaminants in
at Lake Michigan lack of parental female skuas may delay reproduction
attentiveness to eggs in the nest and reduce foetal growth. However,
Male glaucous gulls in the Arctic have dis-
was suggested to be associated with rupted parenting behaviour and the hormone
there were no significant relationships
organochlorine contaminants, leading levels in their eggs are abnormal. between organochlorines and
to reduced reproductive success, [Photo kindly provided by US Fish and Wildlife reproductive variables in males.
Service]
although reduced reproduction Nevertheless, the proportion of nests
here was also related to intrinsic Other experiments suggest that containing non-viable eggs was high
reduced viability of the egg (Kubiak altered prolactin hormone levels may (47%), although no relationship was
et al,1989). The mating behaviour of also be involved in the decreased found between the parents’ residues
birds elsewhere has been impaired. reproductive success. Prolactin of organochlorine contaminants
For example, altered nest building, is an anterior pituitary hormone, measured and the occurrence of
typified by smaller nests of lower closely associated with reproduction non-viable eggs (Bustnes et al.,2007).
quality, were found in tree swallows and parenting behaviours in birds. Therefore, it may be that several
(Tachycineta bicolour) around the Verreault and colleagues (2008) pollutants not measured may be a
PCB polluted Hudson river in the US looked at prolactin hormone contributory factor, or that other
(McCarty and Secord,1999). levels and the concentrations of factors are involved.
16
MALES UNDER THREAT
2.4
birds Altered sex-related
(cont)
characteristics and potential
reduced reproduction
Male starlings (Sternus vulgaris)
exposed experimentally to
environmentally relevant levels of
oestrogen mimicking chemicals
develop longer and more complex
songs compared to control males. In
addition, these experimentally dosed
males had reduced immune function.
The study also reported that females Eggshell Thinning in Birds

preferentially chose the more exposed Eggshell thinning is a notorious
males. Although this was not an pollution-related effect on bird
effect which was measured in wildlife, reproduction, and is caused by DDE,
but was derived experimentally, it the degradation product of DDT
can be deduced that inappropriate (for review see Giesy et al.,2003).
choice of mate might lead to possible However, the precise mechanism
population level effects, because of action is still not known. Effects
if these males were less robust in have persisted for many years, and
fighting off infection, their parenting for example, peregrine falcons (Falco
ability could be compromised peregrinus tundrius and anatum
(Markman et al.,2008). sub-species) breeding in the Canadian
Arctic, were reported to have eggshells
Male American robins (Turdus around 10% thinner than eggs
migratorius) from orchards in produced prior to the introduction
British Columbia, exposed in the of DDT (AMAP,2004). This is
wild to elevated levels of DDT and its presumably due to the chemical body
metabolites, had significantly altered burden being passed on to subsequent
brain development, including reduced generations, coupled with the life-
size forebrain and song nuclei. Such time exposure of each generation.
reduction in the areas which are Similarly, in Greenland, thickness of
responsible for song and sexual the shell of peregrine falcon eggs has
behaviour may potentially adversely improved in the time period 1972-
affect reproduction (Iwaniuk et 2003, but even in 2003 it was still
al,2006). evident to some extent (7.8%) (Falk
et al.,2005). In the UK, birds of prey
have not recovered from the onslaught
of pesticides in some areas. For
example, numbers of peregrines have
not recovered in eastern Yorkshire,
and over the last decade there have
been declines in north Scotland,
Northern Ireland and northern
In male American robins from orchards in Wales. It is thought that persecution,
Canada, the areas of the brain used for mating
and song have been damaged by pollutants.
pollutants, and possibly lack of food
[Kindly provided by ©Albert Steen-Hansen may be restricting the population
Denmark] (RSPB,2007).
17
MALES UNDER THREAT
2.5
mammals Predator mammals in contaminated In mammalian species the following
areas are at risk, because effects, which are discussed in
bioaccumulative contaminants more detail below, have been
can build up in the food chain. noted. In rodents: reduced sperm;
Furthermore, part of the mother’s reduced testes weight and reduced
body burden of man-made chemicals reproduction. In otters and/or
is transferred to the offspring in the mink: reduced baculum (penile
womb and during suckling. Even bone) length; smaller testes and
mammals in a remote area like the impaired reproduction. In seals and/
Arctic are under threat, because or sea lions: impaired reproduction
persistent organic pollutants are (including implantation failure,
carried to the northern latitudes on sterility, abortion, premature
air and ocean currents, in a process pupping). In cetaceans: reduced
termed global re-distillation. Indeed, testosterone levels; impaired
chemical contamination in many reproduction; and hermaphrodite
Arctic predator species is already organs. In polar bears: intersex
at levels above those which have features and deformed genitals;
been reported to cause effects on reduced testes and baculum length;
reproduction in other mammals reduced testosterone levels in adult
(AMAP,2004). males; and reduced cub survival. In
black bears: undescended testes. In
the Florida panther: undescended
testes; altered hormone levels;
abnormal sperm and low sperm
density. In deer: antler deformities;
undescended testes; and testicular
abnormalities, including cells
predictive of testicular cancer. In
eland (an antelope): abnormal testes,
including impaired spermatogenesis.
It has been estimated that almost 1

in 4 mammalian species are at risk
of extinction (IUCN,2008a). Many
factors are to blame, particularly
including habitat degradation, but
First born calves of Florida bottlenose dolphins get most pollutants from their mothers and have lower nevertheless this highlights the need
survival rates than subsequent offspring.
to protect mammalian reproductive
[©iStockphoto.com-Derek Burke]
capability.
18
MALES UNDER THREAT
2.5
mammals Feral Rodents
(cont)
Studies on rodents living in highly Otters

contaminated areas show effects on
reproduction and the testes. For The Eurasian otter (Lutra Lutra) is
example, significantly reduced testes the most widely distributed of all 13
weights have been reported in male species of otters, and is found in the
white footed mice (Peromyscus UK and elsewhere. Several decades
leucopus) inhabiting PCB and ago, otters (Lutra lutra) completely
cadmium contaminated land. disappeared in some UK and
Effects on reproduction were also European rivers, due to contaminant
noted, with numbers of juveniles induced reproductive problems
and sub-adults reduced compared (Mason and Macdonald,2004).
to an unexposed population (Batty Monitoring in 1989-1991 suggested
et al.,1990). Similarly, a study of that at least in some areas, PCBs
striped mice (Rhabdomys pumilio) were still sufficiently high to exert
from a contaminated South African detrimental effects on some UK otters
nature reserve reported two male (Mason and Macdonald,1994). In
animals without any sperm, and addition to the deleterious effects
other animals with relatively low of PCBs and other organochlorine
mean cauda epididymal sperm count contaminants, habitat destruction has
(Bornman et al.,2007). Other rodent also had a negative impact (see EA,
species reported to be affected by 2003).
pollutants, include meadow voles
(Microtus pennsylvanicus) from the After populations of otters plummeted
infamous Love Canal waste site at in Europe, captive bred otters were
Niagara Falls. Reduced population released in some river catchments in
density and reduced seminal vesicle the UK, and elsewhere (Fernandez-
weight were reported in male animals Moran et al.,2002), and otters are
from this polluted site compared to now breeding again. In some UK
animals from a cleaner site (Rowley et rivers the population growth has been
al.,1983). slow (Mason and Macdonald, 2004),
although otter populations are now
expanding over much of Europe.
Nevertheless, the Eurasian otter is still
recognised by IUCN (International
Union of Nature Conservation) as
‘near threatened’ (IUCN,2008b). In
some European countries, such as
Denmark, the distribution range
of the otter was reported to be still
much reduced (Pertoldi et al.,2001).
Similarly, in southern Sweden, total
PCB concentrations are still high
and the indications of population
improvement are weak (Roos et
al.,2001). Overall, in the EU, the
Male striped mice from a polluted nature reserve in South Africa have been found with no sperm. otter population distribution is still
[©iStockphoto.com-Nico Smit] reduced, and as well as PCBs and
19
MALES UNDER THREAT
other organochlorine contaminants, abnormally small reproductive organs, In the UK, the Environment Agency
rodenticides are also a concern in and these reproductive tract disorders funds post mortem examination of
some areas (Fournier-Chambrillon et correlated with several environmental otters found dead, mainly due to
al.,2004). contaminants present in the river road kill, in England and Wales. One
(NBS,1996). Research by Henny and unilateral cryptorchid male otter
colleagues reported that the baculums was found in 1994, and although
and testicles of young males from the no further males with undescended
Lower Columbia River were shorter testes were reported in the 600
or smaller than in animals of the or so found dead in south west
same age group from non-polluted England (Simpson,2008), a study of
areas. In the Portland Vancouver male otters from southern England
area, where the highest PCB and showed smaller baculum length
organochlorine levels were recorded, in young otters was correlated to
of the four animals collected, one higher levels of organochlorine
otter even had no testicles. However, contaminants in their livers. Out of
it was suggested that some of the the 195 males examined, abnormally
Otters in Europe have suffered reduced repro- effects on the young male river small or distorted baculi were seen
duction, and males with undescended testes
have been found in the UK. otters from the Lower Columbia in 7 otters, with the otter from
[Kindly provided by ©Hugh Jansman, Alterra] River might be temporary, resulting Hampshire having both a small
from delayed development due to penis and unusually small testes
Sea otters have also declined in some endocrine dysfunction (NBS,1996). (Simpson,2007). However, these
areas, including the southern sea otter In addition, it may be that PCBs are results need careful interpretation. In
(Enhydra lutris nereis) population in not responsible for the effects on the depth examination of the testes from
California and the Alaskan sea otters baculum of the otter, but are just a more than 250 or so male otters found
(E. lutris kenyoni) in the Aleutian ‘tracer’ for other pollutants, because dead, which have been frozen and
Islands, USA, but the reasons for this an experiment in which growing stored in a ‘bio-bank’ serving much
are unknown (Hanni,2003). mink were fed Arochlor 1254 PCB did of England and Wales, could provide
not report any effect on their baculi more information as to whether
The North American river otter (Aulerich et al.,2000). the reproductive health of male
(Lontra canadensis) also presently otters in the UK was compromised.
occupies a greatly reduced range, and However, in 2008 in the UK more
at least 17 states and one Canadian otters with undescended testes have
province have undertaken re- been found than in previous years
introduction programmes (Kimber (Chadwick,2008). Early in 2008,
and Kollias, 2000). Chemical one otter from Humberside was
pollutants have been suggested as a found with both testes undescended,
possible cause of the decline in both and subsequently two other otters
Europe and North America (Conroy et with unilateral cryptorchidism were
The range of North American river otters has
al.,2000; Wren,1991). reduced. In a polluted river, males with smaller found in the summer of 2008, one in
Structural defects of the male baculums and testicles have been reported. Cumbria, and one in Hertfordshire
reproductive tract have been reported [Kindly provided by ©Nicole Duplaix] (Chadwick,2008). More funding
in some studies of male otters. Otters is needed for further detailed
surveyed in the polluted Lower investigation of the bio-banked
Columbia river in North America specimens, and or for in-depth
in the 1990s were reported to have investigation of fresh new specimens.
20
MALES UNDER THREAT
2.5
mammals Mink
(cont)
The endangered European mink In North America, in the 1970s,
(Mustela lutreola) has suffered a commercial mink farms reported
rapid decline, and its distribution reproductive failure in their mink
is still shrinking. In France, the which were fed fish from the Great
range of the mink shrank by Lakes, and it was subsequently
nearly 50% over the last 20 years shown that exposure to low levels
(Fournier-Chambrillon et al.,2004). of PCBs could impair reproduction
Rodenticide exposure via prey in this species. Data from 1982 and
(Fournier-Chambrillon et al., 2004), 1987 from surveys around the Great
and exposure to contaminants such Lakes continued to indicate that wild
as PCBs and other organochlorines mink (Mustela vison) populations
are a concern. It seems that mink were being affected by pollutants,
are particularly susceptible to particularly PCBs (Wren,1991).
reproductive effects due to dioxins Rather alarmingly, recently reported
and structurally related PCBs levels of PCBs in mink from western
(Wren,1991), and to mercury (Basu Lake Erie have increased since
and Head,2008). 1979 when they were last sampled,
and moreover, many exceed the
lowest observable effect level for
reproductive impacts (EC,2003;
Fox,2005).
The Housatonic River in Connecticut,

downstream of an old General Electric
Company plant, is particularly
contaminated with PCBs. Mink fed
fish from this river had offspring with
lower birth weights and higher infant
mortality rates, compared to mink fed
with Atlantic herring, such that it can
reasonably be predicted that the wild
population are likely to be suffering
adverse effects (Bursian et al.,2003).
Structural defects have also been
Mink in Europe have suffered a rapid population decline.
noted. In British Columbia in
[©iStockphoto.com-Frank Leung]
Canada, there was a significant
negative correlation between total
PCB concentrations and baculum
length in juvenile mink, caught in
the winters of 1994/5 and 1995/6,
although individual animals with
gross abnormalities of reproductive
systems did not show high levels of
chlorinated contaminants (Harding
et al.,1999). Moreover, as reported
in the section above on otters, it may
be that PCBs are not the causal agent
for this structural defect, but instead
a marker for other contaminants,
21
MALES UNDER THREAT
because an experiment in which

growing mink were fed Aroclor 1254
PCB did not report any effect on their
baculum (Aulerich et al.,2000).
Seals and Sea Lions
In the 1970s, harbour seals (Phoca or increasing. The role that pollution (see review, Damstra et al., 2002).
vitulina) in the polluted Dutch may play in this is under investigation, Some of the disorders observed in
Wadden Sea (part of the North but whatever the causes it seems that the exposed female seals included
Sea) declined in number, with low they cover a large part of the North abortion in early pregnancy, uterine
reproduction being blamed on Sea as there has been widespread stenosis and occlusions, and sterility
PCBs adversely affecting female population declines ranging from the (Bergman,1999a; Bergman 1999b).
reproductive capability. A study Wash to the Shetland (Lonergan et
showed that female harbour al.,2007). The Sea Mammal Research Moreover, many seals from the
seals fed fish from the polluted Unit at St Andrew’s university is going Arctic, including some ringed
Wadden Sea had half as many pups to look at some parameters related to (Phoca hispida) and northern fur
compared to seals fed fish from the reproductive health of male and seals (Callorhinus ursinus) are
the less contaminated Atlantic female seals captured and released contaminated with summed PCB
(Reijnders,1986). Altered levels in August and September 2008 at levels above the threshold for
of sex hormones were suggested a number of sites. Scottish Natural decreased reproduction in otter
to have led to implantation failure Heritage is funding some research (AMAP,2004).
(Reijnders,1990). to enable the seals found dead to be
subject to investigation, but more In sea lions (Zalophus californianus)
Subsequently, seal populations in funding is needed to fully investigate in the USA stillbirths and premature
Britain and Europe were decimated the potential effects of contaminants pupping were reported in the 1970s,
by outbreaks of phocine distemper on the reproductive health this species and this was associated with high PCB
virus in 1988 and 2002. These (Hall, 2008). and DDE levels (DeLong et al.,1973).
outbreaks caused the deaths of more At this time, on San Miguel Island
than 23,000 and 30,000 harbour some twenty percent of the California
seals respectively and the initial sea lion pups died due to premature
outbreak was suggested to have birth. The p,p’-DDE levels in the
been exacerbated by pollutants premature parturient cows’ blubber
compromising the immune system of were 7.6 times greater than in the full-
the seals (Härkönen et al.,2006; Hall term animals, although it seems that
et al.,1992). Concern about this fish infections may also have contributed
eating mammal is still high. Britain Common seal colonies around Britain have (Gilmartin et al.,1976). In western
holds 40% of the total European declined. Alaska, Steller sea lion (Eumetopias
common or harbour seal (Phoca [©iStockphoto.com-Janne Hämäläinen] jubatus) populations have also
vitulina) population, and the numbers suffered a decline. The cause is not
of harbour seals in eastern England In the Baltic, it is well accepted known, and it may be related to a
have not increased since the end of that pollution has caused reduced decline in their prey, but pollution
the 2002 phocine distemper epidemic. numbers of seals due to reproductive may also be a factor, because these sea
Indeed, there is evidence of a general problems. The seals are reported to lions have been found to have higher
decline in large harbour seal colonies have compromised endocrine systems concentrations of persistent organic
around Britain, apart from the Inner associated with high levels of PCB and pollutants in their excreta, than less
Hebrides where numbers are stable DDT and related chemicals affected populations (AMAP,2004).
22
MALES UNDER THREAT
2.5
mammals Cetaceans (whales, dolphins and
(cont)
porpoise)
Beluga whales (Delphinapterus The beluga population in the St

leucas) in the St Lawrence estuary Lawrence estuary has not increased
and orca whales (Orcinus orca) in the since hunting was banned in the
Northeast Pacific are two very highly 1970s. In a report published in 1995
polluted wildlife populations (for by Douglas, the rate of pregnancy
review see Fossi and Marsili,2003; of beluga whales in the St Lawrence
Heiman et al.,2000; McKinney river estuary was only 3% compared
et al.,2006; Wolkers et al.,2007). with 35% in those from the Canadian
Neither is reproducing well. They Arctic (see Riedel et al.,1997). De
have some of the highest PCB levels Guise (1995) suggested that this
found in wildlife, higher than those could be linked with exposure
associated with reduced reproduction to organochlorines. Scientists
in seals, although the effects of have also reported finding a true
contaminants on whales is difficult to hermaphrodite (with 2 testicles and
ascertain with certainty (Trites and 2 ovaries) (De Guise,1995), and a
Barrett-Lennard,2001). pseudo-hermaphrodite (Mikaelian et
al.,2003).
Beluga whales in the St Lawrence estuary are highly polluted. Reproduction is imparied and hermaphrodites have been found.
[©iStockphoto.com-Klaas Lingbeek- van Kranen]
23
MALES UNDER THREAT
In the Arctic, not only killer whales,

but also some harbour porpoises
(Phocoena phocoena) from Norway,
long-finned pilot whales (Globicephala
melas), narwhal (Monodon
monoceros), and some minke whales
(Balaenoptera acutorostrata) have
summed PCB levels higher than those
associated with decreased otter and
mink reproduction (AMAP,2004).
There has been a decline in harbour

porpoise (Phocoena phocoena)
populations since the 1940s in the
southern North Sea and the English
Channel, and similar declines have
been reported in the rest of Europe. Porpoise numbers have declined. Some stranded animals are contaminated to levels likely to affect
reproduction.
Recent studies mainly suggest that the
[Photo kindly provided by Paul Jepson,©MEM]
pregnancy rate in North Sea porpoise
is lower than in the western Atlantic or
Iceland waters (Pierce et al,2008). At The reproduction of dolphins in effect of PCBs and DDE in reducing
least some of this population decline waters off the USA also seems the testosterone level in Dall’s
is believed to be due to chemical compromised. For example, in porpoise may be an indication of the
contamination of the female. For Sasasota Bay, Florida, female causative effects of PCBs and DDE in
example, a study of stranded animals reproductive success improved with affecting the normal sexual functions
found concentrations of PCBs in age, potentially reflecting depuration of wild animals.”
the fat of female common dolphins of the mother’s pollutants to her
(Delphinus delphis) and harbour first born, and correlating with the Without good base-line data from
porpoises from the Atlantic coast of mother’s PCB load. Only half of unpolluted populations it is difficult
Europe above the threshold at which the first born calves of bottlenose to know whether organ size has been
effects on reproduction could be dolphins (Tursiops truncates) impacted by chemical exposures, but
expected in other mammals (such as survived through their first year, a study of 192 male porpoises found
mink, otter and seals) in 40% of the compared to a 70% survival rate in stranded or caught in commercial
dolphins and 47% of the porpoises. subsequent calves (Wells et al.,2005). fishing nets in UK waters, found no
In the southern North Sea, this rose consistent evidence that any of the
to 74% of porpoises being over the Effects on sex hormones in cetaceans contaminants in the porpoises were
contamination threshold at which have been associated with pollutants. negatively associated with male
reproduction effects could be expected For example, reduction in the reproductive indices (Bennet et
in other mammals. Perhaps not testosterone levels in Dall’s porpoise al.,2003).
surprisingly therefore, the average of the northwestern North Pacific
pregnancy rate recorded in porpoises has been associated with exposure
in the southern North Sea study area to PCBs and DDE, the latter being
was lower than in the western Atlantic, statistically significant (Subramanian
although the scientists cautioned that et al.,1987). The authors considered
the sample size for the southern North that, “irrespective of the precise
Sea was small (Pierce et al.,2008). mechanisms involved, the plausible
24
MALES UNDER THREAT
2.5
mammals Polar Bears
(cont)
Some PCBs have increased in polar The impacts of contaminants on the
bears (Ursus maritimus) in the period Svalbard polar bear population are
between 1967 and 1994 (Derocher et inconclusive but there are suggestions
al.,2003) and similarly, other “newer” of contaminant-related population
contaminants have also increased in level effects that could have resulted
recent years (1984-2006) (Dietz et from reproductive impairment of
al.,2008). Indeed, it is considered females, lower survival rates of cubs,
that pollutants coupled with global or increased mortality of reproductive
warming may pose a threat to the females (Derocher et al.,2003).
long-term survival of this species Cubs of mothers with high levels
(Jenssen,2006). of contaminants in their fat were
found to be more likely to die during
their first year than cubs of mothers
with low levels. These cubs may be
particularly vulnerable since polar
bear milk is about 30 percent fat, and
contaminants stored in the mother’s
fat are transferred to offspring during
suckling. Certainly, the summed
PCB levels in some Svalbard polar
bears exceeded the levels known to
be correlated with poor reproductive
success in seals (AMAP,2004).
Male polar bears in East Greenland with higher levels of organochlorine pollutants were found to have
smaller testes and shorter baculums.
[©iStockphoto.com-David T.Gomez]
25
MALES UNDER THREAT
Intersex / Hermaphroditism and

Reduced Testosterone in Polar
Bears
Scientists have suggested that in organochlorines in male polar bears were over one year old and
polluted areas, hermaphrodite polar throughout their life could therefore were therefore considered to be
bears may be more common, and aggravate any reproductive toxicity cryptorchid. The remaining seven
that this condition could be due that might have occurred during early bears may have had delayed
to excessive maternal androgen development in the womb (Oskam et testicular descent due to immature
excretion caused by a tumour or al.,2003). development. This is the first
endocrine disrupting pollutants (Wiig published report of the prevalence
et al., 1998). In 1996, two yearling The genitalia in male polar bears of cryptorchidism in black bears,
Svalbard polar bears, which were also appear to be damaged by and therefore it is difficult to draw
believed to be female, were found pollutants. Reproductive organs conclusions (Dunbar et al.,1996).
with a normal vaginal opening and a from 55 male East Greenland polar As of 2008, there did not seem to
20 mm penis containing a baculum. bears caught by subsistence hunters be any significant reproductive
Then on subsequent separate were examined to investigate the problems in Florida black bears
occasions, two other Svalbard potential negative impact caused (Cunningham,2008).
bears were found to exhibit female by organohalogen pollutants. There
pseudo-hermaphroditism as they was a significant inverse relationship
had deformed genitals, manifest as between organohalogen contaminants
clitoral hypertrophy (Wiig et al.,1998). and testis length and baculum
However, some of these later reported length and weight. This was found
females may have been mis-diagnosed in both sub-adults (associated with
as pseudo-hermaphrodites, because DDT related chemicals, dieldrin,
a subsequent female was found with chlordanes, hexacyclohexanes,
an enlarged clitoris, with no signs of PCBs, and polybrominated diphenyl
any histological or structural changes ethers (PBDEs)) and adults
Several male black bears in Florida in the
which would be expected if hormone (hexachlorobenzene (HCB)). Baculum
1990s were found to have undescended
disruption was involved (Sonne et bone mineral densities decreased testes.
al., 2005). Nevertheless, subsequent with increasing chlordanes, DDTs, [©iStockphoto.com-Ashok Rodrigues]
studies on 44 female East Greenland and HCB in sub-adults and adults.
polar bears which had been caught It seems that hormone disrupting In bears in Alberta in Canada, a
by subsistence hunters, indicated pollutants are reducing the size of couple of decades ago there were
that contaminants were affecting male East Greenland polar bear some reported cases of masculinized
oestrogen-sensitive female organs. genitalia, and this may pose a risk females, but the cause of this pseudo-
For example, an inverse relationship to this polar bear population in the hermaphroditism was not known
was found between the levels of future because of reduced sperm (Cattet, 1988). Out of 38 black and 4
the sum of some organohalogen and penis size/robustness (Sonne et brown bears collected, 4 female black
contaminants and ovary length and al.,2006). bears and 1 female brown was found
ovary weight (Sonne et al.,2006) to have some degree of male genital
development. Given the frequency
Normal sexual development and later of the occurrence, environmental
reproductive function are dependent Black Bears factors might have played a role. It
on testosterone, and so it is a matter was suggested that excessive maternal
of some concern that the levels of Effects suggestive of sex hormone androgens, herbicides, or plant
some organochlorine contaminants disruption have been reported. For derived alkaloids might have been
in adult male polar bears have example, Dunbar and colleagues involved. However, it is speculated
been linked with perturbation of found retained testes in 11 (16%) of 71 here that atmospherically transported
testosterone levels. Researchers male black bears (Ursus americanus) industrial pollutants could perhaps
have suggested that the continuous examined over a 3-year period in also have played a role.
presence of high concentrations of Florida (USA). Four of the 11 bears
26
MALES UNDER THREAT
2.5
mammals Florida Panther
(cont)
Facemire and colleagues (1995) Deer – Family Odocoileus

reported that many of the small
endangered population of Florida There are several examples of male
panther (Felis concolor coryi) reproductive health problems in deer.
have abnormal sperm, low sperm For example, Veeramachaneni and
density, or undescended testicles. colleagues have reported that many
These effects may be linked to the Sitka black tail deer (Odocoileus
abnormally similar serum oestradiol hemionus sitkensis) on Kodiak Island,
levels found in male and females, Alaska have undescended testicles,
which indicated that many males had and antler dysgenesis, both of which
been de-masculinized and feminized. are signs of defective androgen action.
Endocrine disrupting pollutants, These researchers could not rule out
taken up through the food chain, were a link with a recessive mutation in a
considered to be the possible cause. founder animal, but considered that
However, other researchers have in-utero exposure to one or more
suggested that the effects seen may environmental oestrogen mimicking
be largely due to the genetics of the chemical was more likely to be the
in-bred small population (Mansfield cause.
and Land,2002). Both sterile males
and an infertile female have been In the Aliulik peninsula on Kodiak
reported (Facemire et al.,1995). High Island, two thirds of the deer
Florida panthers have been found with
levels of mercury, PCBs and pesticide examined (61 out of 94) had neither
abnormal hormone levels, reduced sperm and residues have been reported in Florida testicle descended, and 70% of these
undescended testes.
panther (see Florida Fish and Wildlife (43) had abnormal antlers. Another
[©iStockphoto.com-Jonathan Lyons]
Conservation Commission). 7% had one testicle un-descended.
Animals from elsewhere on the
island or from neighbouring islands
were much less affected. The testes
of some of the deer were subject to
examination. Where both testes
were un-descended, there were
many abnormalities, including no
spermatogenesis and carcinoma in
situ (CIS) like cells (considered to be
precursors of seminoma, a form of
testicular cancer) (Veeramachaneni
et al.,2005). Effects on reproduction
at the level of the individual must
therefore be apparent, as those
with neither testicle descended are
azoospermic (without sperm).
27
MALES UNDER THREAT
Mule deer (Odocoileus hemionus)

on a former plutonium production
site along the Columbia River at the
Hanford Site, Washington (USA)
have also been found with abnormal
testes and antlers. Some 27 of 116
adult males examined had unusually
shaped, velvet-covered antlers and
abnormal testes. The severity of
the testicular atrophy and apparent
lack of other affected tissues led the
Many male Sitka black-tailed deer on Kodiak
Island have undescended testes and de- researchers to suggest that radiation
formed antlers. was unlikely to be responsible (Tiller
[Photo kindly provided by et al.,1997).
Dr.James.P.Jacobson]
From 1996 to 2000, accident-

killed and injured white-tailed deer
(Odocoileus virginianus) in Montana Eland
USA were collected and examined for
genital abnormalities. Of the 254 The eland is a large antelope from
male deer examined, approximately the Bovidae family. Deformities
two thirds showed varying degrees reported in eland (Tragelaphus oryx)
of genital developmental anomalies, are believed to be the first evidence
specifically mis-positioned and of terrestrial wildlife being affected
undersized scrota and ectopic by hormone disrupting chemicals in
testes. The authors discussed the South Africa. Professor Bornman and
possible role of endocrine disrupting colleagues collected testes and body Eland in a polluted South African nature
pesticides, but could not give any fat from 24 eland. Focal white gritty reserve have been found with abnormal testes
and impaired spermatogenesis.
firm conclusions as to the cause of the areas were observed in the testes
[©iStockphoto.com- Adrian Assalve]
abnormalities (Hoy et al., 2002). of all eland, and spermatogenesis
was generally impaired (Bornman operations. In some of the eland,
Earlier research by Marburger et al.,2007). The fat samples of the other endocrine disrupting pollutants,
(1967) also reported finding eland contained the oestrogenic including octylphenol, PCB and DDT
genital defects in male white tailed compound p-nonylphenol, and it was related chemicals were also found. A
deer (see Veeramachaneni et al., suggested that the testicular lesions few atypical germ cells were seen, but
2005). Similarly, earlier research observed in eland could be associated detailed morphological evaluation
in Columbian black tailed deer in with this, as the vacuolisation to show carcinoma in situ was not
California (Odocoileus hemionus of sertoli cells were similar to possible because of limitations
columbianus) found effects suggestive those observed in rats exposed to of tissue fixation and processing
of defective androgenic action. nonylphenol (Bornman et al., 2007). (Bornman et al.,2007) These workers
During an 18 year period, 4.1% of Nonylphenol ethoxylate, which breaks concluded that the findings in
male deer had mis-shapen antlers and down to nonylphenol, is used as an eland were similar to the testicular
some had testicular atrophy, but the ingredient in many pesticides, as well dysgenesis syndrome in humans
cause was not determined (De Martini as in leather or textile processing, attributed to developmental exposures
and Connolly,1975). metal working, and cleaning to chemicals.
28
MALES UNDER THREAT
section 3
effects reported
in wildlife
in polluted
environments,
endocrine
disruptors in
the environment
and the mixture
effect
3.1
highly
contaminated
aquatic
environments
Persistent chemicals tend to end up
in water-bodies and oceans, where
elevated levels of bioaccumulating
compounds are found in wildlife at the
top of the food web. Most of the data
on the adverse effects of chemicals in
wildlife come from polluted waters
that have been the subject of in-depth
studies. These particularly include
the Great Lakes, the Baltic and the
Arctic, the latter being particularly
contaminated due to long range
transport of pollutants via air and
ocean currents, in a process called
global re-distillation.
In the Great Lakes basin over 400 man-made chemicals have been found in wildlife, and reproduction
has been impaired in at least 14 species.
[©iStockphoto.com-Jeremy Edwards]
29
MALES UNDER THREAT
In the Great lakes basin, over 400 and Olsson 1985; Bergman 1999a). blood levels that were just 100-fold
man-made chemicals have been found It would appear that many female higher than the blood level found
as wildlife contaminants (EC,1997). seals have been unable to reproduce in humans living in the Canadian
By the early 90s, at least 14 species of because of persistent pollutants Arctic. Many adverse effects were
fish and fish-eating wildlife had been (Bergman,1999), and although the noted in the offspring they produced
reported with reproductive problems, Grey seal (Halichoerus grypus) including growth suppression,
population declines or other adverse population has increased following decreased spleen and thymic weights,
health effects attributed to chemical a decrease in some organochlorine increased serum cholesterol and liver
contaminants (Gilman et al.,1991). levels, problems remain (Nymen et microsomal enzyme activities, lower
These species included snapping al.,2002). In many marine mammals liver retinoid levels, and histological
turtle (Chelydra serpentine), in both the Baltic and the North sea, changes in the liver, thyroid, and
cormorant (Phalacrocorax effects on the immune system is spleen (Chu et al.,2008). Similarly,
auritus) black crowned night heron an ongoing concern, because there experiments feeding farmed Arctic
(Nycticorax nycticorax), bald eagle is evidence to suggest that mass foxes (Vulpus lagopus) with whale
(Haliaeetus leucocephalus), osprey mortalities may have arisen due to a blubber ‘naturally’ contaminated in
(Pandion haliaetus), herring gull reduced ability to fight off infections the wild, has illustrated that wild foxes
(Larus argentatus), ring backed gull (van Loveren,2000; Hall et al.,1992; exposed to an environmental cocktail
(Larus delawarensis), Caspian tern Jepson et al.,2005). of persistent organic pollutants may
(Hydroprogne caspia), common be at risk of developing chronic kidney
tern (Sterna hirundo), Forster’s tern and liver damage (Sonne et al.,2008).
(Sterna forsteri), wild mink (Mustela
vison), otter (Lutra canadensis),
beluga whales (Delphinapterus
leucas) from the St Lawrence river
which is fed by water from the
Great Lakes, and farmed mink fed
Great Lakes fish. Levels of some Helsinki harbour. Seals in the Baltic have had
contaminants have declined since the problems reproducing, and young women are
early 1990s, but concern is still high. advised to limit their consumption of Baltic
fish.
Therefore, in 2001, Environment
[©iStockphoto.com-Dan Mason] Arctic foxes are at risk, because captive foxes
Canada (EC) initiated the first phase fed on whale blubber show many adverse
(2001-2005) of the Fish and Wildlife In the Arctic, levels of contaminants health effects.
Health Effects and Exposure Study, are considered to be above the [Kindly provided by Per Michelsen ©
www.arcticimages.com]
which was to explore the wildlife / threshold for effects in a few wildlife
human health connection. Some species (Fisk et al.,2005). Effects on In the last decade, research funding
fish are still contaminated to an immune system function associated has led to increased knowledge
extent such that it is recommended with contaminants have been reported about the effects of chemicals in the
they should only be eaten in limited in polar bears and humans (for Arctic (Fisk et al.,2005), but there
amounts or not at all. reviews see, Muir et al.,2005; van are concerns in some quarters that
Oostdam et al.,2005). Indeed, for funding for wildlife studies appear
The Baltic has also been the subject other adverse effects safety margins to be now being cut back. The global
of numerous studies as it is relatively may not be sufficient to provide an UNEP Stockholm Convention which
highly contaminated due to its adequate level of protection for the came into force in 2004 has resulted
shallowness and low water exchange. human population. For example, in the phase out, or reduced releases,
The Finnish Food Safety Authority researchers exposed rats to a mixture of some 12 organochlorine chemicals,
has recommended that women of of contaminants that simulates which in turn has reduced some
childbearing age should limit their the blood contaminant profile of levels recorded in the environment
consumption of Baltic herring, salmon humans residing in the Canadian (Chan et al.,2008). However, levels
and predatory fish (see EVIRA,2008). Arctic. Female rats were exposed of other persistent contaminants have
Effects have been found in fish eating during pregnancy and lactation to increased in recent years (Dietz et
wildlife, particularly seals (Bergman this mixture at doses that resulted in al.,2008).
30
MALES UNDER THREAT
3.2
endocrine
disruptors and
mixture effects
Some unidentified chemicals in the discharges of most sewage works tested are able to block the
action of male hormones.
[Photo kindly provided by ©Anglian Water]
Information from laboratory studies

can also be used to assess potential
effects. For example, in the UK it is
a matter of some concern that two
nationwide surveys in 2003, which
assessed the effluent from 43 sewage
treatment works on 2 separate
occasions using the YAS (yeast
androgen assay), have revealed that
77% of samples had anti-androgenic
activity of 50 micrograms per litre
(μg) flutamide equivalent (FE) or
more, 17% had between 300-500 μg/l
FE, and 7% had 500 μg/l FE or more
(Johnson et al.,2007).
Flutamide is an anti-androgenic
pharmaceutical compound which
has been used as a comparative
measure of anti-androgenic activity.
Anti-androgenic pollutants have the
potential to de-masculinise males
and affect their ability to reproduce.
As of November 2008, the chemicals
responsible for the anti-androgenic
activity in the effluents had not
yet been identified. In addition to
contaminants with anti-androgenic
effects, many effluents also contain
chemicals with oestrogenic action
31
MALES UNDER THREAT
and these contaminants have the In laboratory experiments, many Epidemiological and field studies
ability to feminise males. In UK more chemicals have been shown which seek to identify the chemicals
sewage effluents, natural oestrogens, to have sex hormone disrupting that are instrumental in causing
including oestrone and17-oestradiol properties or to affect androgen adverse effects in the wild are
have been found, alongside dependent tissues, and some of these hampered by the fact that there
pharmaceutical oestrogens, such as substances have also been found in are many confounding factors, and
ethinyl oestradiol, used in the birth the environment (EA,1998). For pollutants are ubiquitous. Under
control pill, and these compounds example, some polybrominated natural conditions, it is virtually
typically account for the bulk of diphenyl ethers (PBDEs) (Stoker et impossible to identify individual
the oestrogenic activity in these al.,2005; Darnerud,2008) which have causative agents in mixtures of
discharges. However, several man- had extensive use as flame retardants highly correlated contaminants.
made chemicals with oestrogenic in consumer products, and some Nevertheless, associations can be
action have been found in fresh water PCBs and dioxins are frequently seen between effects and certain
river sediment, including bisphenol found as contaminants in biota (Gray contaminants.
A, octylphenol and nonylphenol et al.,1999a; Kaya et al.,2002; see
(Pottinger et al.,2008). With regard Vreugdenhil et al.,2002) . Moreover, Controlled laboratory experiments
to the marine environment, man- certain phthalates (Howdeshall et continue to play a major part in
made endocrine disruptors have al.,2008) and parabens (Darbre and determination of the potential
been reported in estuaries and Harvey,2008) have been reported causal agent(s). Unfortunately,
discharges, including, for example, to possess anti-androgen activity in however, laboratory studies are
nonylphenol and DEHP (di-(2- animals, as have many pesticides. severely hampered because such
ethylhexyl) phthalate). Higher These include the DDT metabolite, a ‘reductionist’ approach cannot
oestrogenic activity has been found p,p’-DDE, linuron, vinclozolin, embrace the complex multi-causality
in estuarine sediments, as compared procymidone, prochloraz (Rider and stepwise triggers that may impact
to estuarine water, and nonylphenol, et al.,2008; Wilson et al.,2008), on disease in the outside world. For
cinnarizine (an anti-histamine drug) fenarimol (Ankley et al.,2005), example, in the environment the
and cholesa-4,6-dien-3-one (a natural fenitrothion (Katsiadaki et al.,2006), presence of several pollutants, natural
cholesterol degradation product ) chlorpyrifos (Kang et al.,2004), and ecosystem stressors, and other factors,
were positively identified as making ketoconazole (Shin et al.,2006). such as ultra violet light exposure
a minor contribution to this activity. Dieldrin, a persistent pesticide, is (Lyons et al.,2002), may affect the
Nevertheless, the main cause of the also reported to have anti-androgenic toxic response.
oestrogenic activity in estuarine properties in test tube experiments
sediments is unknown (Allen et al., (Fowler et al.,2007). In addition,
2002). There is therefore a need certain pharmaceuticals have de-
for more resources to identify the masculinizing properties, some of
pollutants found in the environment which, such as the drug cimetidine
that are responsible for endocrine used for indigestion and ulcers, may
disrupting activity. leave the body unchanged in urine
or breast milk (Huques et al.,2000;
França, et al.,2000; Hey,2006)
1
Dioxins are chlorinated chemicals which are products of incomplete combustion.
2
Phthalates are used in many consumer products and are found as uniquitous environmental contaminants.
Amongst other things, they are used to make plastics flexible.
3
Esters of p-hydroxybenzoic acid (parabens) have been found in human urine and in human breast
tissue. Parabens is used in many bodycare cosmetics, and is able to penetrate the skin (Darbre and
Harvey,2008)
32
MALES UNDER THREAT
3.2
endocrine
disruptors and
mixture effects
(cont)
Wildlife and humans are exposed to many pollutants. This mixture or so-called ‘cocktail effect’ can
act additively and tip susceptible animals over the threshold for effects.
[©istockphotos.com-Juan Monino]
Mixture Effects of masculinization (Gray et al.,2001;

Wildlife are exposed to many Wilson et al.,2008). Male rodents
compounds concurrently, some of exposed experimentally to such
which act with a similar mechanism anti-androgenic chemicals show a
of action or via mechanisms of cascade of features representative
action that converge. For example, of malformations in male hormone
laboratory experiments have now receptor dependent tissues, including
clearly shown that additive effects shortened ano-genital distance,
can occur due to exposure to more nipple retention, and testes-related
than one chemical. For example, two effects (Gray et al.,1999a). Hass’s
phthalates with a similar mechanism team have also found similar additive
of action, working against the male effects in rodents after exposing
hormone, can give rise to additive them simultaneously to three anti-
effects (Foster et al.,2000). Similarly, androgen mimicking chemicals. An
subsequent experiments have revealed increased number of penile defects
that in rodents, five phthalates show (hypospadias) was found after
additive action, with BBP (benzylbutyl exposure to the mixture, but no such
phthalate), DBP (di(n)butyl increase over normal levels was found
phthalate), DEHP (di(2-ethylhexyl) when each chemical was administered
phthalate) and DiBP (diisobutyl alone at the same concentration as in
phthalate) being equipotent, and the mixture, because individually it
DPP (dipentyl phthalate) being about was below its effect level (Christiansen
3-fold more potent (Howdeshell et et al.,2008)
al.,2008). Furthermore, toxicants can
produce additive effects even when Interactive effects, including additivity
two or more chemicals are acting via or even synergism, also occur with
different mechanistic pathways (Gray other mechanisms of action. For
et al.,2002; Rider et al.,2008). For example, additivity of effects has been
example, certain phthalates inhibit shown in fish exposed to a mixture
testosterone synthesis during foetal of oestrogenic chemicals (Brian et
life, and dioxins alter androgen al.,2005), and similarly Crofton and
dependent tissues, and also the colleagues (2005) have shown that
pesticides vinclozolin, procymidone, when several thyroid disrupting
linuron and the DDT metabolite chemicals are given to rodents, effects
(p,p’DDE) are all androgen receptor can occur even when each chemical
antagonists, which de-rail the process is given at a dose level below their
33
MALES UNDER THREAT
no effect concentration. For thyroid

disrupting chemicals, both additive 3.3
and synergistic effects were reported.
transgenerational
effects
Several workers have shown that Effects due to early life exposures
exposure to pesticide mixtures can may also result in effects on
cause effects greater than single subsequent generations. Several
exposures. For example, Moore and laboratory studies have suggested
Lower (2001) have shown an additive transgenerational effects in both
response in male fish due to exposure invertebrates and vertebrates. A
to a weak mixture of atrazine and transgenerational effect is an effect
simazine pesticides (0.5ppb each), which is carried across generations
which caused reduced milt expression as a consequence of events that
in fish because of altered olfactory happened during the lifetime of the
function and reduced reaction to previous generation. Such effects
female pheromones. Similarly, Hayes have been seen in fish (Gray et
and co-workers have shown effects on al.,1999b), and also in mammals. For
the immune system in frogs exposed example, in rodents, an increased
to low levels of several pesticides incidence of cancer has been
(Hayes et al.,2006). noted in the granddaughters and
grandsons of mice exposed to DES
Organisms are most vulnerable to when pregnant (Newbold et al.,1998;
the effects of EDCs during early life 2000). Similarly, an increased risk
development in the uterus or in the of hypospadias has been reported
egg, and during puberty, particularly in the sons of women exposed in-
when cell fate is determined utero to DES (Brouwers et al.,2005).
and differentiation is occurring. Furthermore in rats, deficits in sperm
Moreover, there may be a substantial production and infertility have been
delay before the effects from early shown in 3 subsequent unexposed
life exposures are seen. Effects from generations, as well as in the first
exposures prior to birth or hatching offspring exposed to methoxychlor or
can range from gross structural vinclozolin while in the uterus of
defects to subtle, but important, the mother rat. It seems that this is
behavioural effects. This delay not due to a mutation in the gene,
between exposure and effects further but instead due to altered DNA
hampers the identification of which methylation, which then causes
chemicals are involved. changes in the expression of a gene or
genes in a process termed epigenetic
reprogramming (Anway et al.,2005).
However, the effect with vinclozolin
was not found in a subsequent study
by industry scientists (Schneider
et al.,2008). Nevertheless,
transgenerational effects of diet are
found (Painter et al.,2008), such
that more work is certainly needed to
understand how contaminants may
affect future generations
34
MALES UNDER THREAT
section 4
conclusions and
recommendations
Conclusions from findings in
wildlife
There is very good evidence More resources are needed to ensure
that pollutant related effects are better monitoring of contaminants
widespread in male vertebrate and their effects in wildlife in
wildlife. Some of the most prevalent locations throughout the globe.
effects reported in male wildlife, There is a need to ensure that wildlife
which are associated with pollutants, populations are sustainable, and that
are related to genital disruption enough males are contributing to the
(GD). GD includes an array of next generation in order to maintain
manifestations. Notable amongst genetic diversity. Wildlife research is
these are: intersex features (such vital not only for wildlife conservation
as egg tissue in the testes of the itself, but also to provide insight into
male); small phallus; small testes; potential effects in humans.
undescended testes or other obvious
structural defects of the male
reproductive tract; or ambiguous
genitals. Genital disruption has been Implications for human health
reported in males of some species Taken together, the effects seen
of wild fish, amphibians, reptiles, in wildlife should raise concerns
mammals, and to a lesser extent, for contaminant induced genital
birds. In addition, in egg laying disruption in human male infants.
species, including fish, reptiles, and Indeed a condition called testicular
birds, abnormal production of egg dysgenesis syndrome, including birth
yolk protein, VTG, has been recorded defects of the penis of baby boys,
in males. All these effects can be cryptorchidism (undescended testes),
caused by exposure to sex hormone reduced sperm production and
disrupting pollutants in the womb, or testicular cancer, has been suggested,
in the egg. The effects reported show because there is evidence to indicate
many similarities across vertebrate that these effects may be interlinked
species, as outlined in Table 1. in causation (Skakkebaek et al.,2001;
2007; Sharpe and Skakkebaek,2008).
Moreover, in many studies these
disorders or demasculinization
effects have been associated with
exposure to certain contaminants or
sex hormone disrupting chemicals
in humans (Hendersen et al., 1976;
Gill et al.,1977; Hosie et al.,2000;
Baskin et al.,2001; Swan et al.,2003;
Pierik et al.,2004; Swan et al.,2005;
Bornman et al.,2005; Hardell et al.,
2006; Damgaard et al.,2006; Main
et al.,2006; Paris et al.,2006; Main
et al.,2007; Fernandez et al.,2007;
Andersen et al.,2008; Bonde et
al.,2008; Brucker-Davis et al.,2008;
McGlynn et al.,2008; Swan,2008).
Scientists have also noted that the
35
MALES UNDER THREAT
rapid pace of the increase of human exposure to the single substance a substitution plan must then be put
male reproductive disorders indicates under consideration is below its no in place.
an environmental cause (Skakkebaek effect level. Unfortunately, such an
et al., 2001), as do studies following approach would not be protective, As of the end of November 2008, the
baby boys born to immigrants who because many chemicals to which updated EU Regulation on pesticides
take on the same risk for testicular humans and wildlife are exposed exert was not finalised and was still the
cancer, as the offspring of residents oestrogenic or anti-androgenic action, subject of on-going negotiations.
born in that country (Myrup et and therefore there is a heightened CHEM Trust believes that EU usage
al.,2008). If testicular dysgenesis potential for additive effects from of endocrine disrupting pesticides
syndrome is occurring in humans due endocrine disrupting chemicals. Even should be phased-out and safer
to pollutants, then genital disruption when individual substances are below alternatives found, particularly
should be found in wildlife in areas their so called no effect concentration, for those which persist in the
with high levels of pollutants, and this derived from experiments on a environment or which give rise to
indeed does seem to be the case. limited number of rodents, effects human exposure.
could occur in populations at large,
Implications for regulation due to several substances acting The potential for transgenerational
Current findings merit urgent action additively. Furthermore, some effects also increase the concern,
to drastically reduce exposure to researchers consider that there may and underlines the need for a more
chemicals of very high concern, anyway be no threshold for effects for robust approach to regulation.
such as EDCs, and persistent and some hormonally active chemicals More research is warranted to fully
bioaccumulating chemicals. CHEM (Sheehan,2006). Within large understand the long term effects
Trust believes that eliminating populations, it might be conjectured from exposure to low levels of
exposure and using safer alternatives that there will be some who, due to contaminants, and particularly to
is the best way forward. their baseline hormone levels, will understand the science of epigenetics
experience adverse effects. and the impact chemical exposures
The new EU Regulation on may have on subsequent generations.
industrial chemicals, called There is to be a mandatory review
REACH (Registration, Evaluation, of how EDCs are dealt with under
Authorisation and Restriction of REACH by June 2013. At this
Chemicals), which came into force in review, CHEM Trust believes any
June 2007, ensures that chemicals further initial authorisations for the
with endocrine disrupting properties use of substances with endocrine
can be subject to prior authorisation. disrupting properties should be
This means that such chemicals may blocked if there are safer alternatives.
have to be phased-out unless they are In the meantime, it is nevertheless
specifically authorised for a particular important that Member States and the
use. However, firstly, a Member Commission urgently put substances
State or the Commission would have with these undesirable properties
to instigate the drafting of a dossier forward for authorisation, even if
with a view to bringing the endocrine the current legislative text may allow
disrupting chemical on to the their use to continue in the short
candidate list for prior authorisation. term. This is because the current
Moreover, as it is currently worded, text of REACH dictates that when
it seems that endocrine disruptors authorised substances come up for
included under the authorisation re-authorisation, if the update of the
procedure will be permitted to be used analysis of alternatives shows that
provided that there is indeed a suitable alternative,
36
MALES UNDER THREAT
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EFFECTS OF POLLUTANTS ON THE REPRODUCTIVE HEALTH

OF MALE VERTEBRATE WILDLIFE -

A CHEM Trust report by Gwynne Lyons

CHEM Trust is committed to engaging with all parties, including regulatory

CHEM (Chemicals, Health and Environment Monitoring) Trust

Further copies of this report can be downloaded free from

Section 2: Pollutant-Related Effects Reported in Male Vertebrate Wildlife and

Section 3: Effects Reported in Wildlife in Polluted Environments, Endocrine

Section 4: Conclusions and Recommendations.

Abbreviations and Technical Terms.

 BHC alpha benzene hexachloride (related to Lindane insecticide)

Section 2 summarises the effects

Reduced Intersex / Deformities VTG Other Sex

VTG production in several wild male

A USA survey of bullfrogs (Rana

Male snapping turtles from polluted sites in the

Decreased hatching success has also Alligators

Turtles living in polluted sites

Here, abnormal testes, including chemicals, following a spill in the

Male red-belly turtles in Lake Apopka in Florida

Abnormal VTG Production in

Deformities of the Reproductive

Szczys and colleagues (2001) noted

More recently, pollutant-related eight persistent organohalogen

The study also reported that females Eggshell Thinning in Birds

It has been estimated that almost 1

Studies on rodents living in highly Otters

The Housatonic River in Connecticut,

because an experiment in which

Seals and Sea Lions

Beluga whales (Delphinapterus The beluga population in the St

In the Arctic, not only killer whales,

There has been a decline in harbour

Intersex / Hermaphroditism and

Facemire and colleagues (1995) Deer – Family Odocoileus

Mule deer (Odocoileus hemionus)

From 1996 to 2000, accident-

Information from laboratory studies

Mixture Effects of masculinization (Gray et al.,2001;

no effect concentration. For thyroid

References Beasley V.R. (2008) Email pers.comm. to

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