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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 419: 121–128, 2010
doi: 10.3354/meps08872 Published November 30
INTRODUCTION
The effects of pollution on wildlife and other organ-
isms in the Arctic marine environment are of great
concern, as many pollutants can have long-term
impacts on reproduction, embryo development,
growth or in other ways pose a risk to the health of ani-
mal populations (Attrill & Depledge 1997, Matthiessen
& Law 2002, Wu et al. 2005). Despite this concern,
there are very few toxicity studies for polar marine spe-
cies, vertebrate or invertebrate (Chapman & Riddle
2005). Benthic amphipods have potential as sensitive
bioindicator organisms of contaminant-induced effects
in marine ecosystems (Thomas 1993), and are also
widespread in Arctic environments.
The economy of Greenland, like most Arctic areas, is
highly dependent on marine ecosystem services since
a large part of the human population hunts and fishes
locally. Given that most of Greenland’s exports are also
based on fisheries, the maintenance of both local food
supply and the economy is highly reliant on the protec-
tion of the marine local habitats. However, the long-
range transport of contaminants (Lockhart 1995, Riget
et al. 2004), together with structural changes in Green-
land leading to more centralized consumer and indus-
trial activities, have resulted in a larger and more geo-
graphically concentrated discharge of contaminants
into the marine ecosystem.
One method to assess effects of contamination is
through the use of bioindicator organisms, which are
any kind of species whose function, status or popula-
tion productivity can be used to determine the state of
the ecosystem they inhabit (Adams 2005). For the West
Greenland marine ecosystem we suggest the benthic
© Inter-Research 2010 · www.int-res.com*Email: liso@ruc.dk
Local anthropogenic contamination affects
the fecundity and reproductive success of an
Arctic amphipod
Lis Bach1, 2,*, Astrid Fischer1, 3, Jakob Strand1
1Department of Marine Ecology, National Environmental Research Institute, Aarhus University, Denmark
2Department of Environmental, Social and Spatial Change, Roskilde University, Denmark
3Department of Toxicology, Wageningen University and Research Centrum, Wageningen, The Netherlands
ABSTRACT: This study investigates whether adaptation to life in contaminated Arctic areas carries a
cost for the populations in terms of reduced fecundity and reproductive success. The benthic amphi-
pod, Orchomenella pinguis occurs in huge densities in both clean and contaminated sites. O. pinguis
was collected at contaminated sites in an open fjord adjacent to Sisimiut, West Greenland, and at
clean sites outside the fjord exposed to open waters. The broods of gravid females were analyzed for
number of embryos, embryonic developmental stage and number of embryo abnormalities. Further,
a sample from 3 of the sites was sexed and analyzed for intersex occurrence. The individuals col-
lected at the most contaminated site had significantly higher fecundity (i.e. reproductive potential),
but also higher frequency of embryo aberrations resulting in lower fertility (i.e. actual reproductive
success) compared to clean site individuals. These results indicated a cost of living in highly contam-
inated environments in terms of reduced reproductive success. This study confirms the potential of
the benthic amphipod O. pinguis as a bioindicator for assessments of reproductive effects of contam-
inants in the Arctic marine environment.
KEY WORDS: Orchomenella pinguis · Embryo development · Embryo aberrations · Greenland
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 419: 121–128, 2010
amphipod Orchomenella pinguis (Lysianassidae) as a
useful bioindicator species, since it is a highly common
macroinvertebrate in the area (Bach et al. 2009). Fur-
ther, O. pinguis is, like other lysianassid species, im-
portant in the benthic food chain where it forms an
essential link by decomposing organic matter and as a
food item for vertebrate predators such as fish and
birds (De Lange et al. 2005, Ide et al. 2005). In addition,
this species is relatively stationary, present in huge
densities, easy to sample and has a circumpolar distri-
bution (Horner & Murphy 1985, Sainte-Marie 1986a,b,
1991, Legezynska et al. 2000, Bach et al. 2009).
Contaminants can have a wide range of effects on
marine organisms. Several studies have reported im-
pacts of contaminants on reproductive success in
amphipod populations, including embryo aberrations
(Sundelin & Eriksson 1998, Camus & Olsen 2008, Sun-
delin et al. 2008b, Pastorinho et al. 2009) and reduced
fertility resulting from the occurrence of intersex (Ford
et al. 2003a,b, Ford & Fernandes 2005). Amphipods are
model organisms for reproductive studies. They are
easy to examine as there is no pelagic larval phase and
embryos are carried maternally in a ventral brood
pouch (marsupium) from fertilization of the eggs to
their emergence as fully developed juveniles. Amphi-
pods have thus been recommended as useful bio-
indicator species to assess effects of contaminants on
invertebrate reproduction (Sundelin et al. 2008a).
The fjord Ulkebugten (Sisimiut, West Greenland) is
impacted by untreated wastewater from different
sources including households (approximately 5500 in-
habitants), a hospital, a fish factory, and other indus-
tries, as well as a great deal of boat, trawler and cruise
traffic. This has resulted in a fjord contaminated
with e.g. polycyclic aromatic hydrocarbons (PAHs) and
heavy metals (Bach et al. 2009; summarized in
Table 1). However, at all sites (including inside the har-
bor and at the hospital wastewater outlet) where sam-
pling was attempted, Orchomenella pinguis occurred
in large densities despite high contamination levels,
indicating that this species has high capacity to adapt
to live in contaminated environments. As a study area,
this fjord was ideal because of the availability of sites
with different contamination inputs in close vicinity
(max. 5 km) to clean sites.
This study is based on previous findings of dense
occurrences of O. pinguis at both clean and highly con-
taminated sites (Bach et al. 2009). The overall objective
of this study was to investigate if adaptation to life in
contaminated areas carries a cost in terms of reduced
fecundity (i.e. reproductive potential) and impaired
fertility (i.e. actual reproductive success) for popu-
lations of the Arctic benthic dwelling amphipod,
Orchomenella pinguis, in the fjord Ulkebugten, Sisim-
iut, Greenland.
122
Site GPS positions Sediment Sediment Organic Depth Sum of Copper Cadmium Mercury Lead TBT
grain size color content (%) (m) 16 PAHsa
Hospital 66° 56.584’ N, 53° 39.169’ W Silty Dark/black 4.00 5–10 1050 23 0.38 0.21 6.3 7
Marina 66° 56.611’ N, 53° 39.528’ W Small grained Dark grey 1.70 10–15 290 12 0.13 0.03 3.2 6
Harbor 66° 56.000’ N, 53° 40.093’ W Silty Black 5.60 5–10 12 900 130 0.61 0.35 33.1 523
Outer Bay 66° 56.529’ N, 53° 41.229’ W Grained Grey 0.80 5–10 20 6 0.11 0.01 1.3 >1
Frederik VII’s Island 66° 55.857’ N, 53° 45.447’ W Grained Grey 1.10 5 –10 8.2 6 0.05 0 1.3 3
North Bay 66° 57.453’ N, 53° 46.323’ W Grained Grey 0.50 5–10 nd 6 0.09 0 1.0 >1
aAccording to the list of the 16 important PAHs designated by the US Environmental Protection Agency— see Bach et al. (2009) for details
Table 1. Summary of contamination in sediment samples from 6 sites after Bach et al. (2009) and additional tributyltin (TBT) analyses. Average measurements of samples
taken in October 2006, August 2007 and August 2008: organic content, sum of polycyclic aromatic hydrocarbons (PAHs) (µg kg dry wt–1), copper, cadmium, mercury and
lead (mg kg dry wt–1), and TBT (µg kg dry wt–1). nd: not determined
Bach et al.: Contaminant effects on amphipod reproductive success
MATERIALS AND METHODS
Study area. Orchomenella pinguis was sampled in
August 2008 in Ulkebugten, an open fjord in Sisimiut
on the western coast of Greenland. Six sampling sites
(Fig. 1) were selected based on knowledge of local
contamination sources and levels (summarized in
Table 1) from a previous study (Bach et al. 2009) and
additional data for tributyltin (TBT) analyzed as
described by Strand et al. (2006). Three sites (sites 1 to
3) are located within the fjord, close to point sources:
(1) the Hospital outlet, (2) the Marina and (3) inside the
Harbor. One site, (4) Outer Bay, is located facing the
open waters, outside town but close to the small air-
port. The 2 reference sites (5) Frederik VII’s Island and
(6) North Bay were located outside the fjord and
exposed to the open water masses. All sites were
within a distance of ~5 km from each other and equally
influenced by tides, temperature (~6°C) and a stable
salinity (~33).
Sampling and analyses. Amphipods were sampled
overnight using traps baited with fish tissue. In most
cases, this sampling method provided more than a
thousand individuals in each catch. The amphipods
were kept in large buckets (10 l) in cold, aerated sea-
water and supplied with sediment and algae (Ulvae
sp.) as natural substrates and cover until processing.
Shortly after sampling, a number of brood bearing
females from each site was sorted from the overall
sample consisting of juveniles, males and mature
females. Gravid females were easily recognized
because they appear more stocky than males and non-
gravid females and because eggs and embryos in the
marsupium showed through the coxal plates as a
red/purple mass. A picture was taken of the gravid
females using a dissection microscope with a camera
attached for later measurements of individual body
length (anterior end of the cephalon to the distal end of
the telson) using an image analysis program (SigmaS-
can Pro version 5.0.0). Eggs and embryos were gently
removed from the living females and the number,
developmental stage and frequency of embryo aberra-
tions per brood per female were scored for each
female. Embryonic stages were categorized as shown
in Fig. 2, after Sundelin & Eriksson (1998), with spe-
cies-specific modifications.
The aberrations found in embryos in this study
(Fig. 3) included twin eggs, undifferentiated eggs and
embryos with ceased development, oedema and
impaired membranes, and other non-specific aberra-
tions; they were similar to those described by Sundelin
et al. (2008a) and found by Camus & Olsen (2008). A
high frequency of pale embryos was found in the
broods of Harbor females, which themselves were
somewhat paler than females from other sites. A small-
scale study based on ex vivo cultivation of pale em-
bryos from the Harbor, resulted in high frequency of
later-occurring aberrations, total arrest in embryonic
stages or delayed development; all with less output of
vital juveniles compared to a parallel study with
embryos from the North Bay where a 100% normal
output was found. As a result of these findings the pale
embryos were categorized as aberrations.
The term ‘embryo’ is used synonymously with egg
throughout the manuscript and thus also includes
early-stage unfertilized eggs. Based on previous hatch-
ing experiments, embryos were also classified abnor-
mal if the developmental stage was ≥2 stages delayed
compared to the rest of the embryos in the brood. For
analysis of results, all types of aberrations were catego-
rized as one group. To distinguish between severity of
embryo aberrations per female, the percentage was
calculated and indexed into >2 – 5%, >5 – 20%, >20 –
50% and > 50 – 100% embryo aberrations per female.
Differences between sites for female size and brood
size were tested by the non-parametric Kruskal-Wallis
test, since assumptions of normality and
homogeneity of variances could not be
met. Site differences in the frequencies
of broods with embryo aberrations
were tested with 2 ×2 contingency
tables and followed by a χ2test.
The intersex analysis was restricted to
3 sites: Hospital, Harbor and North Bay.
After removal of gravid females, sub-
samples of the samples from these sites
were prepared. From each sub-sample, a
number of individuals (34, 44 and 42, re-
spectively) was sorted under a stereo mi-
croscope and divided into males, mature
females, immature females (i.e. with
rudimentary brood plates) and juveniles.
Gender and intersex occurrence were
123
Fig. 1. Sampling sites in Sisimiut, Greenland, 2008. Locations range from the
inner part of the fjord Ulkebugten to open waters. Three sites are close to point
sources of contamination: (1) Hospital outlet, (2) Marina, and (3) the Harbor.
One site: (4) Outer Bay, faces open water but is close to the small airport. Two
reference sites are exposed to open water masses: (5) Frederik VII’s Island and
(6) North Bay
Mar Ecol Prog Ser 419: 121–128, 2010
analyzed after Ford et al. (2003b), where intersex was
classified as presence of rudimentary brood plates and 1
or 2 genital papillae. Site differences in the gender and
intersex occurrence were tested with 2 ×4 contingency
tables and followed by a χ2test.
RESULTS
The embryonic stages for Orchomenella pinguis
were comparable to those described by Sundelin &
Eriksson (1998) and used by Camus & Olsen (2008) on
124
Fig. 2. Orchomenella pinguis. Characterization of embryonic development of O. pinguis. Seven embryonic stages of embryogen-
esis were adapted: (1) oval blastocytes, red eggs in early cleavage stages, but with no clear structure; (2) small fracture, formation
of the caudal furrow; (3) widening of the caudal furrow and appearance of appendages rudiments; (4) dorsal organ is formed and
the embryo is characterized by a comma shape and segmentation of appendages; (5) appendages and eye pigments become visi-
ble and the embryo is shaped like a half moon; (6) dorsal organ has decreased and the embryos have clearly developed red eyes;
(7) hatched juveniles inside brood chamber, potentially free swimming
Fig. 3. Orchomenella pinguis. Pictures of embryo aberrations (indicated by arrows) show examples of undifferentiated eggs and
embryo arrests, twin eggs and differentiated embryo pigmentation. Aberration types are ab: undefined aberrations; ea: embryo
arrest (dead); m: membrane impaired; p: pale (dead) and tw: twin eggs
Bach et al.: Contaminant effects on amphipod reproductive success
individuals of Monoporeia affinis and Gammerus wilk-
itzkii, respectively. However, for O. pinguis the embry-
onic development was categorized into only 7 stages as
the blastocytes in the early cleavage stages were
grouped into one (Fig. 2).
Brood size
Females carrying broods were in the sizes of 6.4 to
13.4 mm and the average number of embryos per
female was 20 ± 10 (± SD; range: 3 to 44). As the
females from the Harbor were significantly larger
(Kruskall-Wallis: p < 0.05) than from any of the other
sites, and as a relation between size and number of off-
spring previously has been described for other amphi-
pods (Nelson 1980, Ford et al. 2003a), data were
normalized by division by female length (mm). A com-
parison of the mean brood size per female (normalized
to female length) for each site (Table 2) shows that
despite the normalization the Harbor females still car-
ried significantly larger broods than females at any of
the other sites (Kruskall-Wallis: p < 0.01), with females
at Outer Bay and the reference sites (Frederik VII’s
Island and North Bay) carrying the smallest broods.
Brood size in the Harbor was also larger when speci-
fied to each embryonic stage. Further, slightly more
embryos occurred in the early stages 1 to 2 than in the
later stages 5 to 7 at most sites.
Embryo aberrations
The percentage of females carrying broods with
aberrations (Fig. 4) was significantly higher (2 ×2 con-
tingency table: p < 0.01) in the Harbor (49%) compared
to all other sites, i.e. Marina (11%), Hospital (12 %),
Outer Bay (0%) and the 2 reference sites Frederik VII’s
Island (0%) and North Bay (16%).
The Harbor site was furthermore the only site with
females carrying broods with more than 20% abnor-
mal embryos (Fig. 4). The highest occurrence of aber-
rations in Harbor embryos was found in broods at the
later embryonic stages 4 to 6, where the average fre-
quency of embryo aberrations per brood reached 25 to
43% (Fig. 5).
Intersex
Among the studied specimens, no observations of
female or male intersex at any of the sites were made
(Fig. 6). There were however small differences, though
none statistically significant, in the frequency of imma-
ture females between clean and contaminated sites.
125
Site n Length (mm) Brood size Normalized Normalized number of embryos in each stage of development
(no. of embryos) brood size (no. of
Mean Range Mean Range embryos mm FL–1)1 2 3 4 5 6 7
Hospital 17 8.4 ± 1.2 6.4– 11.3 14 ± 6.5 3–29 1.7 ± 0.8 3.0 ± 0.8 1.7 ± 1.2 0 1.5 ± 0.5 1.2 ± 0.3 1.4 ± 0.7 0
Marina 28 9.2 ± 0.9 7.5– 10.9 19 ± 8.5 4– 39 2.1 ± 0.8 2.5 ± 0.3 1.3 ± 0.6 2.6 ± 0.7 3.9 2.4 ± 0.4 1.7 ± 0.7 0.5
Harbor 61 10.5 ± 1.0* 8.0 – 13.1 30 ± 7.7* 8–44 2.8 ± 0.6* 2.7 ± 0.7 3.0 ± 0.6 2.9 ± 0.6 2.6 3.0 ± 0.6 2.5 ± 0.7 0
Outer Bay 42 9.1 ± 1.1 6.7– 11.8 15 ± 7.3 4– 35 1.6 ± 0.8 2.0 ± 1.0 1.7 ± 0.5 1.1 ± 0.6 1.9 ± 0.8 1.3 ± 0.1 1.5 ± 0.6 1.2 ± 0.2
Frederik VII’s Island 10 9.0 ± 0.7 7.8– 9.7 11 ± 6.7 3 –23 1.2 ± 0.7 1.8 ± 0.3 0 0 1.9 ± 0.7 0.4 0.6 ± 0.2 1.1 ± 0.3
North Bay 43 8.3 ± 0.7 6.9–10.5 14 ± 6.0 5 –35 1.7 ± 0.6 2.6 ± 0.4 1.5 ± 0.4 1.9 ± 0.8 1.4 ± 1.8 1.8 ± 0.3 1.8 ± 0.7 1.5 ± 0.4
Table 2. Orchomenella pinguis. Data from brood-bearing females at 6 sample sites: number of individuals, n; mean ± SD and range of female body length (FL, mm) and
brood size; brood size normalized by dividing by female body length; and normalized number of embryos per brood in the 7 stages of embryonic development. *p < 0.05
(Kruskal-Wallis)
Mar Ecol Prog Ser 419: 121–128, 2010
Adding the 2 female groups: mature and immature
females, but excluding the undifferentiated group (and
the already sorted gravid females), more females than
males were found at the Hospital and Harbor (63:37
and 61:31, respectively) while the gender distribution
was equal (50:50) in North Bay.
DISCUSSION
The reproductive patterns of Orchomenella pinguis
were studied at contaminated and clean sites. Brood
size, embryonic developmental stages and number of
eggs over embryo aberrations as well as gender and
incidences of intersex were recorded. All parameters
used can be negatively affected by contamination and
may carry costs in terms of reduced fertility as result
of e.g. smaller brood sizes, lower embryo survival,
delayed maturation and reduced pairing success (Sun-
delin & Eriksson 1998, Ford & Fernandes 2005).
A small fraction of the sampled individuals was
gravid females. Occasionally the gravid females were
found with full ovaries with unfertilized oocytes as
well, confirming that Orchomenella pinguis is itero-
parous as suggested by Sainte-Marie (1990). While the
size of the gravid females corresponded to the size of
gravid females collected in Saint Lawrence Estuary
(Sainte-Marie 1990), the broods were found to be
much smaller in the present study. This may reflect dif-
ferences in food availability or a combination of geo-
graphical life history differences. Even within the pre-
sent study, differences in body and brood size were
found for different sites. At the most contaminated site,
the Harbor, amphipod females were larger than the
females collected at the other sites, and even after nor-
malizing to length these females still carried larger
broods. Whether this is an effect of larger body size,
higher food availability or is an attempt to overcome
the higher degree of aberrations found in broods at this
site can only be speculated. However, the finding con-
tradicts the ‘cost of stress hypothesis’ by Calow & Sibly
(1990), whereby smaller broods are hypothesized to
occur in stressed individuals due to reallocation of
energy from growth and reproduction towards stress
defenses. Another factor which can affect the brood
size of amphipods is a potential loss of embryos from
the brood either resulting from active rejection of
dead/malformed embryos or due to abnormal brood
126
0
10
20
30
40
50
60
Hospital Marina Harbor Outer
Bay
Frederik
VII's Island
North
Bay
>2–5%
>5–20%
>20–50%
>50–100%
12% 11%
49%
16%
0 % 0 %
% Females with aberrations
% Aberrations
0
10
20
30
40
50
1234567
Developmental stage
Fig. 5. Orchomenella pinguis. Percentage embryo aberrations
at each developmental stage for the (f) Hospital, (n) Marina,
(d) Harbor and (×) North Bay. See Fig. 2 for developmental
stages
% Distribution
0
10
20
30
40
50
Males Adult
females Females with
rudimentary
brood plates
Juveniles Intersex
Hospital (n = 34)
Harbor (n = 44)
North Bay (n = 42)
Fig. 6. Orchomenella pinguis. Gender and intersex distribu-
tion for the Harbor, Hospital and North Bay samples
Fig. 4. Orchomenella pinguis. Percentage of females within
each site carrying broods with aberrations (see Fig. 3). The
degree of aberrations is indexed within each brood into
>2–5 %, > 5 –20%, > 20–50 % and > 50 –100% embryo aberra-
tions per female
Bach et al.: Contaminant effects on amphipod reproductive success
plate development (Ford et al. 2003a). This might be
the reason for the slightly smaller brood sizes observed
in the later embryonic stages 4 to 6 at most of the sites
in Ulkebugten.
The findings of high levels of embryo aberrations in
the broods of Harbor females, and to a lesser degree in
Hospital, Marina and North Bay females, indicate pol-
lution effects, and are as such in agreement with the
studies by Sundelin & Ericsson (1998) and Camus &
Olsen (2008). Both found severe damage in embryos of
amphipods collected near an aluminum smelter with
high PAH concentrations and in embryos exposed to
PAHs under laboratory conditions, respectively. While
contaminants in general can cause malformed em-
bryos, exposure to hypoxia may result in dead eggs
and embryos (Sundelin et al. 2008a, and references
herein). Particularly high levels of PAHs have been re-
ported from the Harbor in Ulkebugten (Bach et al. 2009;
Table 1) and these may, alone or in conjunction with
other contaminants such as TBT, have triggered the
high frequency of embryo aberrations in Harbor broods
in the present study. TBT was also found in high con-
centrations in the Harbor sediments and though no
studies, to our knowledge, have addressed the direct
effects of TBT on amphipod embryo development, re-
productive effects of TBT have been found in e.g. fish
larvae (Fent & Meier 1992, Bodammer 1993).
Though the evidence for embryo aberrations was
only really strong at the Harbor site (49%), there were
also lower frequencies of broods with aberrations at
the Hospital (12%), Marina (11 %) and North Bay
(16%), which are higher than the assumed back-
ground levels of 5% in amphipods (Sundelin et al.
2008a). The findings for the Hospital and Marina cor-
respond to the contamination levels at these sites,
which are elevated but lower than in the Harbor. The
occurrence of broods with embryo aberrations at the
reference site North Bay cannot be explained by the
measured contamination levels, but may be attributed
to other contaminants.
Regarding intersex, other studies report observa-
tions of intersex in amphipods from contaminated sites
related to direct contamination effects, incomplete
feminization by microsporidian parasites, or as a con-
sequence of environmental sex determination (Ford et
al. 2003b, Ford & Fernandes 2005). In the present
study, there were no indications of development of
intersex in Orchomenella pinguis in individuals from
the 3 sites studied. Females with rudimentary brood
plates are suggested by Ford et al. (2003b) to represent
a form of endocrine dysfunction, similar to that of inter-
sex, as they are often observed in populations with
high incidence of intersex. Whether the finding of the
higher frequency of females with rudimentary brood
plates in both Hospital and Harbor compared to the
clean site (North Bay) is due to natural differences in
amphipod maturation processes and/or to contamina-
tion effects as suggested by Ford et al. (2003b) and
thus in the category of intersex, is unclear at present.
The impact of contaminants on the amphipods and in
particular on their fecundity may not only affect indi-
viduals but the overall population size and productivity
over the long-term. As amphipods are brooders and
carry their young in a brood pouch until they hatch
as fully developed juveniles, contaminants affecting
adults will also affect their offspring as they are re-
leased into the same environment. This can be expec-
ted to have consequences in terms of slower recruit-
ment and/or re-colonization. The Harbor population
may already have experienced such population-level
effects. The sampling in August 2008 and an additional
sampling in 2009 yielded much fewer individuals at
the Harbor site that at earlier samplings in August 2006
and August 2007 (Bach et al. 2009); this is indicative of
recent environmental changes, and severe pollution
events like oil spills cannot be excluded.
These results indicate a cost of living in highly conta-
minated environments in terms of reduced reproductive
success, shown by an increase in embryo aberrations,
possibly accompanied by the development of different
reproductive strategies to overcome that cost. For future
studies of the costs of living in contaminated areas in
terms of reproduction, other parameters such as time to
reproduction onset, embryo development time and juve-
nile growth and survival are suggested to be included.
Further field and laboratory studies are also needed to
evaluate if the reproductive changes in the amphipods
can be mainly attributed to contaminants or if other en-
vironmental stressors also have significant effects.
CONCLUSION
The Orchomenella pinguis sample collected at the
most contaminated site in the Harbor, had higher fre-
quency of broods with embryo aberrations compared
to samples from cleaner reference sites and also from
less contaminated sites. However, the Harbor females
also produced larger broods; but whether this has
evolved as a reproductive strategy to overcome the
greater embryonic loss or is an effect of higher food
accessibility remains unclear. A larger suite of environ-
mental stressors should be included in future studies to
enable separation of environmental influences from
the effects of contaminants.
Acknowledgement. We thank A. Willumsen and staff at
Department of Arctic Technology, Technical University of
Denmark, and Sanaartornemik Illiniarfik for providing
research facilities in Sisimiut, Greenland.
127
Mar Ecol Prog Ser 419: 121–128, 2010
LITERATURE CITED
Adams SM (2005) Assessing cause and effect of multiple
stressors on marine systems. Mar Pollut Bull 51:649–657
Attrill M, Depledge MH (1997) Community and population
indicators of ecosystem health: targeting links between lev-
els of biological organisation. Aquat Toxicol 38: 183–197
Bach L, Forbes VE, Dahllöf I (2009) The amphipod Orchome-
nella pinguis — a potential bioindicator for contamination
in the Arctic. Mar Pollut Bull 58:1664–1670
Bodammer JE (1993) The teratological and pathological
effects of contaminants on embryonic and larvae fishes
exposed as embryos: a brief review. Am Fish Soc Symp 14:
77–84
Calow P, Sibly RM (1990) A physiological basis of population
processes: ecotoxicological implications. Funct Ecol 4:
283–288
Camus L, Olsen GH (2008) Embryo aberrations in sea ice
amphipod Gammarus wilkitzkii exposed to water soluble
fraction of oil. Mar Environ Res 66:221–222
Chapman PM, Riddle MJ (2005) Toxic effects of contaminants
in polar marine environments. Environ Sci Technol 39:
200A–207A
De Lange HJ, De Haas EM, Maas H, Peeters E (2005) Conta-
minated sediments and bioassay responses of three
macroinvertebrates, the midge larva Chironomus riparius,
the water louse Asellus aquaticus and the mayfly nymph
Ephoron virgo. Chemosphere 61:1700 –1709
Fent K, Meier W (1992) Tributyltin-induced effects on early
life stages of minnows Phoxinus phoxinus. Arch Environ
Contam Toxicol 22:428–438
Ford AT, Fernandes TF (2005) Notes on the occurrence of
intersex in amphipods. Hydrobiologia 548:313–318
Ford AT, Fernandes TF, Rider SA, Read PA, Robinson CD,
Davies IM (2003a) Measuring sublethal impacts of pollu-
tion on reproductive output of marine Crustacea. Mar Ecol
Prog Ser 265:303–309
Ford AT, Fernandes TF, Rider SA, Read PA, Robinson CD,
Davies IM (2003b) Reproduction in the amphipod,
Echinogammarus marinus: a comparison between normal
and intersex specimens. J Mar Biol Assoc UK 83:937–940
Horner R, Murphy D (1985) Species composition and abun-
dance of zooplancton in the nearshore Beaufort Sea in
winter-spring. Arctic 38:201–209
Ide K, Sasaki K, Omori M (2005) Food intake and digestion in
the scavenging lysianassid gammaridean Scopelocheirus
onagawae. Fish Sci 71:721–730
Legezynska J, Weslawski JM, Presler P (2000) Benthic scav-
engers collected by baited traps in the high Arctic. Polar
Biol 23:539– 544
Lockhart WL (1995) Implications of chemical contaminants for
aquatic animals in the Canadian Arctic: some review com-
ments. Sci Total Environ 160-161:631–641
Matthiessen P, Law R (2002) Contaminants and their effects
on estuarine and coastal organisms in the United King-
dom in the late twentieth century. Environ Pollut 120:
739– 757
Nelson WG (1980) Reproductive patterns of gammeridean
amphipods. Sarsia 65:61–71
Pastorinho MR, Telfer TC, Soares AMVM (2009) Amphipod
intersex, metals and latitude: a perspective. Mar Pollut
Bull 58:812– 817
Riget F, Law RJ, Hansen JC (2004) The state of contami-
nants in the Greenland environment. Sci Total Environ
331:1–4
Sainte-Marie B (1986a) Effect of bait size and sampling time
on the attraction of the lysianassid amphipods Anonyx
sarsi (Steele & Brunel) and Orchomenella pinguis (Boeck).
J Exp Mar Biol Ecol 99:63– 77
Sainte-Marie B (1986b) Feeding and swimming of lysianassid
amphipods in a shallow cold-water bay. Mar Biol 91:
219–229
Sainte-Marie B (1990) Reproductive bionomics of some shal-
low-water lysianassoids in the Saint Lawrence Estuary,
with a review on the fecundity of the Lysianassoidea
(Crustacea, Amphipoda). Can J Zool 68:1639–1644
Sainte-Marie B (1991) A review of the reproductive bionomics
of aquatic gammaridean amphipods: variation of life his-
tory traits with latitude, depth, salinity and superfamily.
Hydrobiologia 223:189–227
Strand J, Glahder CM, Asmund G (2006) Imposex occurrence
in marine whelks at a military facility in the high Arctic.
Environ Pollut 142:98–102
Sundelin B, Eriksson AK (1998) Malformations in embryos of
the deposit-feeding amphipod Monoporeia affinis in the
Baltic Sea. Mar Ecol Prog Ser 171:165–180
Sundelin B, Eriksson Wiklund AK, Ford AT (2008a) Biological
effects of contaminants: the use of embryo aberrations in
amphipod crustaceans for measuring effects of environ-
mental stressors. ICES Tech Mar Environ Sci 41
Sundelin B, Ford A, Jacobson T (2008b) Using embryo and
reproductive abnormalities in amphipods to assess the
impact of an ironwork. Mar Environ Res 66:53
Thomas JD (1993) Biological monitoring and tropical biodi-
versity in marine environments:a critique with recommen-
dations, and comments on the use of amphipods as bio-
indicators. J Nat Hist 27:795– 806
Wu RSS, Siu WHL, Shin PKS (2005) Induction, adaptation and
recovery of biological responses: implications for environ-
mental monitoring. Mar Pollut Bull 51:623– 634
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Editorial responsibility: Hans Heinrich Janssen,
Oldendorf/Luhe, Germany
Submitted: September 16, 2009; Accepted: October 11, 2010
Proofs received from author(s): November 28, 2010
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