J OURNAL OF C RUSTACEAN B IOLOGY, 33(6), 793-801, 2013
POPULATION STRUCTURE OF THE HADAL AMPHIPOD HIRONDELLEA GIGAS
(AMPHIPODA: LYSIANASSOIDEA) FROM THE IZU-BONIN TRENCH
Ryan M. Eustace 1 , Niamh M. Kilgallen 2,∗ , Nichola C. Lacey 1 , and Alan J. Jamieson 1,∗∗
1 Oceanlab,
Institute of Biological and Environmental Science, University of Aberdeen,
Main Street, Newburgh, Aberdeenshire AB41 6AA, UK
2 National Institute of Water and Atmospheric Research (NIWA), 301 Evans Bay Parade, Wellington 6021, New Zealand
ABSTRACT
The population structure of Hirondellea gigas (Birstein and Vinogradov, 1955), collected by baited trap from 8172 and 9316 m in the IzuBonin Trench (NW Pacific) was examined. Specimens were categorized according to sex and life stage. At 8172 m, juveniles comprised
the overwhelming majority of the population, whilst at 9316 m the male: female: juvenile ratio was more evenly distributed, suggesting
vertical ontogenetic structuring. Furthermore, juveniles from 8172 m were significantly smaller than those from 9316 m with an average
body length of 11.1 mm (±4.6 S.D.) compared to 19.8 mm (±3.1 S.D.). Females and males showed the opposite trend to juveniles, with
both the largest individuals and the greatest proportion of males and females occurring at 9316 m, no 6 nor brooding females were
captured. Female reproductive strategies and the environmental drivers of ontogenetic structuring of H. gigas populations are discussed.
We conclude that pressure per se does not drive the observed trends but rather an interaction between depth (pressure) and topographyinfluenced distribution of resources in terms of both quality and quantity.
K EY W ORDS: Amphipoda, deep sea, Hirondellea gigas, populations
DOI: 10.1163/1937240X-00002193
I NTRODUCTION
There are currently sufficient datasets from hadal depths to
confirm that necrophagous amphipods play a key role in
the hadal food web, by providing prey to larger organisms
in the upper trench (<8000 m) (Jamieson et al., 2009a,
b) and by their complete dominance of the scavenging
community at depths greater than 8000 m (Hessler et al.,
1978; Blankenship et al., 2006).
The success of Amphipoda in the hadal trenches can be attributed to efficient adaptations to this low-food environment
at high pressure (Jamieson et al., 2010). These adaptations
include: 1) the ability to rapidly localize, and characterize
food sources (Dahl, 1979; Kaufmann, 1994; Tamburri and
Barry, 1999); 2) the ability to feed on large muscular food
sources including the ability to consume large quantities of
food in relatively short periods of time (Shulenberger and
Hessler, 1974; Dahl, 1979); 3) the ability to maximize (store)
the energy derived from high-energy resources such as carrion for gradual utilization over extended periods (Yayanos
and Nevenzel, 1978; Smith and Baldwin, 1984; Perrone et
al., 2003); 4) the capacity to supplement their diet with alternative food sources made available between large carrion
fall opportunities, thereby exhibiting extreme trophic plasticity (Blankenship and Levin, 2007; Kobayashi et al., 2012);
5) the physiological capability to adapt to high hydrostatic
pressure (Yayanos et al., 1981; MacDonald and Gilchrist,
1982; Yayanos, 2009). The energy that is then acquired as a
∗ Present
result of these adaptations can be allocated based upon their
current life stage, whereby more energy is allocated to gonad development and other associated sexual characteristics
during sexual maturity and reproduction or to growth in juveniles (Thurston, 1979; Ingram and Hessler, 1983).
Amphipods are known to rapidly locate and consume
baits placed on the seafloor which simulate the natural occurrence of surface derived carrion-falls, which in theory
should reach the trench floor irrespective of depth (Hessler
et al., 1978; Jamieson et al., 2010). Observed trends across
the bathymetric range of the hadal zone (6000-11 000 m)
are relatively consistent between trenches studied whereby
amphipod diversity decreases with depth, yet the abundance
increases remarkably beyond 8000 m (Blankenship et al.,
2006). The amphipod assemblages in these deeper areas
are dominated by Hirondellea spp. (Lysianassoidea: Hirondelleidae) therefore constituting the most important scavenging fauna at hadal depths (Blankenship et al., 2006;
Blankenship and Levin, 2007). Hirondellea are represented
in the hadal SE Pacific (Peru-Chile Trench) by a currently
undescribed species (Perrone et al., 2002). In the SW Pacific
trenches, Hirondellea dubia Dahl, 1959 dominates, whereas
in the NW Pacific trenches H. gigas (Birstein and Vinogradov, 1955) dominates.
The population structure of most hadal amphipods is
not fully understood as most reports are derived from
collections from a single depth, thus omitting trends which
may occur over their full bathymetric range (Hessler et
address: Australian Museum, 6 College Street, Sydney, NSW 2010, Australia.
author; e-mail: [email protected]
∗∗ Corresponding
© The Crustacean Society, 2013. Published by Brill NV, Leiden
DOI:10.1163/1937240X-00002193
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 33, NO. 6, 2013
al., 1978; Perrone et al., 2002; Thurston et al., 2002). The
exception to this is Blankenship et al. (2006) who reported
the ontogenetic vertical stratification of H. dubia in the SW
Pacific trenches (Kermadec and Tonga).
Hirondellea gigas is thought to be endemic to the northwestern Pacific trenches and has only been recovered from
depths exceeding 6500 m (Wolff, 1960; Beliaev, 1989). Furthermore, studies on inter-trench phylogenetics has revealed
that populations of H. gigas from the Philippine, Palau and
Mariana trenches are isolated from one another (France,
1993), supporting the hypothesis that they are unable to survive outside of the hadal trench environment.
Detailed studies on the population structure of H. gigas
have only been reported from a narrow depth range (96009800 m) in the Philippine Trench (Hessler et al., 1978)
and therefore little is known about its ontogeny. Here the
population structure of H. gigas from the Izu-Bonin Trench
in the NW Pacific Ocean at depths of 8172 m and 9316 m
are described.
is situated under the North Pacific Subtropical Gyre, West (NPST-W)
biochemical province (Longhurst et al., 1995), which is estimated to have
an annual primary production rate of 109 g C m−2 year−1 . The trench has
a maximum depth of 9810 m (Beliaev, 1989), is approximately 1000 km
long, and has a projected area at the 6000 m contour of 99 801 km−2 .
The trench is known to have bottom water temperatures of 1.54°C at
7305 m and 2.36°C at 9180 m (Beliaev, 1989). Bottom currents range from
a southward flow of 3.6, 4.6, and 2.4 cm s−1 , at depths of 4500, 6000 and
9000 m on the western flank of the trench and a northward flow of 3.0 and
12.8 cm s−1 at 9000 and 6000 m respectively on the eastern flank (Fujio et
al., 2000).
Equipment
Study Site
Two deployments of a benthic lander were made on the western flank in
the southernmost tip of the trench at 8172 and 9316 m at approximately
27°N by 143°E (Table 1), with the latter on the trench axis. The samples
were collected using Hadal-Lander A; a free fall autonomous baited lander
equipped with a time-lapsed video system (Jamieson et al., 2009a). On
each of the three lander legs was a 2-litre funnel trap baited with blue-fin
tuna, Thunnus thynnus (Linnaeus, 1758). The traps were 300 mm long by
60 mm diameter, with a trap opening of 25 mm diameter. A temperature and
pressure sensor (SBE-39; Seabird Electronics, USA) recorded every 30 s
throughout the deployments. Pressure data recorded in dbar was converted
to depth (m) following Saunders (1981). The recovered amphipod samples
were fixed in 99% ethanol and later transferred to 70% ethanol after the
expedition.
The study site was in the Izu-Bonin Trench (also known as the IzuOgasawara Trench), east of the Bonin Islands in the NW Pacific Ocean
(Fig. 1). The Izu-Bonin trench runs approximately north to south between
the more northerly Japan Trench and southerly Volcano Trench. The trench
Amphipods were identified to the lowest rank possible following Barnard
and Karaman (1991). Samples of H. gigas from each depth were separated
M ATERIALS AND M ETHODS
Amphipods
Fig. 1. Map of the sampling location in the Izu-Bonin Trench southeast of Japan, near the Bonin Islands in the NW Pacific Ocean. The sampling area is
indicated by the circles.
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EUSTACE ET AL.: POPULATION BIOLOGY OF HADAL AMPHIPODS
Table 1.
Details of the deployment sites in the Izu-Bonin Trench (NW Pacific).
Date
17 Mar 2009
18 Mar 2009
Latitude
Longitude
Depth (m)
Temp. (°C)
Bottom time (hh:mm)
27°22.09N
27°20.99N
143°13.49E
143°18.89E
8172
9316
1.98
2.2
12:28
11:46
by sex; males were identified by the presence of penal papillae between
pereionite 7 and pleonite 1, females were identified by the presence of
oöstegites on the coxae of gnathopod 2 and pereiopods 3 to 5 and specimens
lacking both oöstegites and penal papillae were assumed to be juveniles.
Individuals who displayed both male and female sexual characteristics,
i.e., individuals with both penal papillae and oöstegites were classified as
inter-sex specimens. Using the criteria defined by Hessler et al. (1978)
developmental stages of males and females were assessed (Table 2).
Examination under a compound microscope allowed identification of setae
on oöstegites and the presence of calceoli on the flagellum of antenna 2 in
males. It became apparent that the females did not possess setae on their
oöstegites until 5; consequently 4 of Hessler et al. (1978) was adapted to
include oöstegites of comparable size but without setae.
Following sex and developmental stage analysis, a randomised subsample of 100 individuals (where possible) of males, females and juveniles
were measured and weighed to establish length-weight relationships for
total populations at each depth followed by sex and stage relationships
therein. The specimens were then blotted dry for one minute and weighed
to the nearest 0.0001 g. From here they were laid straight and using digital
callipers measured from the base of the first antennae to the tip of the
telson to an accuracy of 0.1 mm. Any curve in the body which could not
be straightened was measured separately and then added to the total length
data.
R ESULTS
The lander successfully recovered amphipods and recorded
environmental data from both depths. The pressure was
recorded as 8400 and 9586 dbar, which corresponded to a
depth of 8172 and 9316 m respectively. At these respective
sites, the bottom temperature was 1.98 and 2.20°C. Due
to a power failure, the video camera was unable to obtain
any footage from 8172 m. The video data from 9316 m
showed swarms of scavenging amphipods and a conspicuous
presence of the predatory amphipod Princaxelia jamiesoni
Lörz, 2010 (see Jamieson et al., 2012).
The traps only recovered amphipod specimens. The total
number of scavenging amphipods captured at 9316 m was
4050 individuals of which H. gigas accounted for 98%
(n = 3968) and two undescribed species of Tryphosella
(Amphipoda: Lysianassidae) accounted for 2% (sp. A =
41; sp. B = 40). At 8172 m, some 1095 amphipods were
recovered of which H. gigas accounted for 51.3% (n =
647), and the same two undescribed species of Tryphosella
Table 2.
as those recovered from 9316 m accounted for 48.7% (sp.
A = 435; sp. B = 13). In addition, a single specimen of P.
jamiesoni was also recovered from 9316 m. P. jamiesoni is
an ambush predator and not a scavenger which may explain
why only one was caught in the traps and yet so many were
seen on the video (Jamieson et al., 2012). The sample size
of H. gigas made available for this study was a random subsample of 717 individuals from 9316 m and all samples from
8172 m (n = 647).
At both depths juveniles were the most abundant followed
by males and then females, but the number of males,
females and juveniles from 9316 m was more evenly
distributed when compared to those from 8172 m where
juveniles accounted for 96.5% of the total sample (Table 3).
Furthermore there was a large difference in size shown in
the length-frequency distributions (Fig. 2C, F), with the
average body length of juveniles from the two depths being
significantly different (F(1,198) = 252.43, p < 0.001). The
average juvenile length from 9316 m was 19.8 mm ± 3.1
S.D. whilst juveniles from 8172 m had an average body
length of 11.1 mm ± 4.6 S.D.; an increase of 78% from the
shallow to deep juveniles. At both depths males and females
had similar length-frequency distributions (Fig. 2A, B, D,
E), although the average length of females was marginally
larger in both cases; 9316 m = 26.9 mm ± 3.9 S.D. (F),
25.3 mm ± 4.4 S.D. (M) and at 8172 m = 22.5 mm ± 3.5
S.D. (F), 21.3 mm ± 3.6 S.D. (M). However, only in the case
of females and males from 9316 m was there a significant
difference (F(1,198) = 7.53, p = 0.007). The lengths ranged
from 19.5-31.0 mm (F) and 17.3-28.2 mm (M) at 8172
and 17.5-36.6 mm (F) and 17.0-33.3 mm (M) at 9316 m
(Table 4). A comparison of average male length between
depths proved significant (F(1,112) = 10.84, p = 0.001) as
did that of females (F(1,107) = 10.77, p = 0.001).
The resulting power curves (Fig. 3) show that for any
given length greater than ∼18 mm H. gigas from 9316 m
will weigh more than those from 8172 m. However, since
there are so few data for male and female H. gigas caught
at 8172 m the resulting power line is heavily influenced by
Developmental stages of H. gigas. Adapted from Hessler et al. (1978).
Stage
Description
/1
2
3
4
5
6
2
3
No visible penile papillae or oöstegites.
Oöstegites appear as a rounded dot at the base of the pereiopods 3 to 5.
Minute oöstegites protrude from gnathopod 2 and pereiopods 3 to 5.
Oöstegites are elongate and of relatively uniform diameter.
Oöstegites are larger than at 4 and possess setae.
Oöstegites are curved at the distal end and possess setae notably larger than 5
Penile papillae are present but calceoli are absent from the flagellum of the second antenna.
Calceoli are present on the flagellum of the second antenna which is more elongate.
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Table 3.
Population structure of H. gigas from the Izu-Bonin Trench.
Depth
(m)
Female
Male
Juvenile
Ratio
(F:M:J)
Total no.
specimens
9316
8172
160
9
249
14
308
624
1:1.56:1.93
1:1.56:69.3
717
647
juveniles. Likewise the juvenile trend lines for each depth
are very close to one another, supporting the theory that there
is no increase in weight in H. gigas from 9316 m compared
to those at 8172 m.
As a result of developmental stages 1 and 1 being
indistinguishable and therefore classified as juveniles it was
not possible to calculate percentage growth between /1
and /2. Between 2 and 3, an increase in body length
and decrease in percentage growth equalled that of females
(Fig. 4). Only single specimens of 4 and 5 were found, and
these were both from 9316 m. There were no 6 collected
from either depth.
There was only one inter-sex specimen found which was
from 9316 m (Fig. 3). The specimen had well developed
penal papillae but was lacking any calceoli on the second
antennae and had oöstegites (of corresponding morphology
and size to 3) present on gnathopod 2 and pereiopod 4. It
Fig. 2. Frequency histograms of H. gigas body length for both sampling depths. A, B and C represent females (n = 9), males (n = 14) and juveniles
(n = 100) respectively at a depth of 8172 m, whilst graphs D, E and F represent females (n = 100), males (n = 100) and juveniles (n = 100) from 9316 m.
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EUSTACE ET AL.: POPULATION BIOLOGY OF HADAL AMPHIPODS
Table 4.
Length (mm) data for each developmental stage of H. gigas at both depths.
Depth (m)
8172
9316
Max
Mean
Min
Max
Mean
Min
/1
2
3
2
3
4
5
6
Intersex
17.7
11.1
1.7
25.7
19.8
10.8
28.6
21.3
17.3
31
25
16
–
–
–
33.3
30.2
26
–
–
–
25.6
22.6
17.1
24.2
21.4
20.1
33.5
28.3
24.5
–
31.0
–
–
36.2
–
–
–
–
–
37
–
–
–
–
–
–
–
–
–
–
–
35.6
–
was also the third largest H. gigas individual examined from
either depth.
In addition to specimens of H. gigas, copious loose
oöcytes were also recovered from 9316 m. None of the loose
oöcytes were held by females in any great number and were
simply loose in the containers or caught in between the
pereiopods and ventral surface. The oöcytes varied in size
from 0.27 mm to 1.1 mm in diameter. The volume of the
oöcytes was calculated ((4/3)πr 3 ) and log10 transformed,
returning a range of 7.0-8.8 μm3 . The majority of the
oöcytes had a faint orange tinge, but some (of intermediate
size) were more heavily pigmented than the rest.
D ISCUSSION
These new data provide evidence that despite the presence
of both mature and juvenile H. gigas towards the deepest
parts of the trench, there is still ontogenetic vertical stratification. Juveniles were the most dominant life stage of H.
gigas found at 8172 m with their percentage of the total
population diminishing with depth (Fig. 5). The presence
of both mature and juvenile individuals at all stations (this
study and Hessler et al., 1978) suggests that the vertical stratification is not driven by depth (or pressure) per se, but rather
by another environmental driver in combination. It is unlikely that temperature is influencing this trend as despite
a slight warming of bottom waters with depth, the temperature range is very low; ∼1°C increase across the depth range
of the trench (3800 m). Salinity was also found to be constant (34.69 ppt) throughout the hado-pelagic water column.
It is therefore more likely that food supply and other associated ecological interactions drive ontogenetic stratification.
This is supported by Blankenship et al. (2006) who reported
similar ontogenetic stratification for H. dubia and Scopelocheirus schellenbergi Birstein and Vinogradov, 1958, with
food availability suggested as a major contributing factor.
Necrophagous amphipods such as H. gigas are seemingly
reliant on surface derived food falls for their survival
(Blankenship and Levin, 2007). These come in two forms,
particulate organic matter (POM) and large food falls which
may be terrestrially derived as well as originating from
various depths of the ocean (Wolff, 1976; George and
Higgins, 1979; Kobayashi et al., 2012). The nutritional value
of the falling POM decreases with increasing depth due to
pelagic heterotrophs selectively removing labile compounds
including proteins, fatty acids and phytopigments (Wakeham
et al., 1984; Beliaev, 1989; Sokolova, 1994; Jamieson et
al., 2010). Large food falls, whilst far more scarce, may
largely be unaffected by depth and could potentially reach
the seabed with the same or similar nutritional quality as
they originated with (Robison et al., 2005; Billet et al., 2006;
Jamieson et al., 2010). Moreover, the food supply in hadal
trenches must be considered within its topographical setting.
The area of seafloor habitat (within a trench) decreases
with depth, thus the total amount of surface-derived food
delivered to the trench will also decrease with increasing
depth. This suggests that the shallower depths of hadal
trenches present the greatest quantity (largest surface area)
and quality (less pelagic uptake) of organic matter. However,
in addition to the steady rain of POM and food falls, the
trenches host a unique influence on the distribution of food
in the form of intermittent seismic events. These influences
should in theory funnel organic matter towards the trench
axis creating a higher density of organic matter, albeit
on a smaller area (Itou, 2000; Otosaka and Noriki, 2000;
Danovaro et al., 2003; Romankevich et al., 2009; Glud
et al., 2013). These seismic induced downward sediment
displacement events have been recorded in the neighbouring
Japan Trench during the 1994 Sanriku-Oki earthquake
(Mw = 7.7; Itou et al., 2000). In the neighbouring
Ryukyu Trench and Kuril-Kamchatka Trench to the north,
an accumulation of organic matter was found with increasing
depth (Itoh et al., 2011), a trend also suggested to occur
in the Peru-Chile Trench (Mazzola et al., 1999). These
observations all suggest that there is a resource gradient with
the trenches.
Why are juvenile H. gigas most abundant at shallower
depths? Likewise, if amphipods are descending with age,
culminating with the most mature individuals at the deepest
point, what mechanisms are there for juveniles to gather
at shallower depths? It is not known if females migrate
up the trench slopes to release their brood, or if juveniles
independently move up the trench. If juveniles are to move
such relatively large distances then they would need to have
high fat reserves in order to fuel such a large migration. This
is partially supported by the known high lipid content of
H. gigas (Yayanos and Nevenzel, 1978), however, it would
seem impractical for a female to supply such a high quantity
of energy to a large brood in an energy-poor environment
and with large food falls being scarce and ephemeral the
opportunity for juveniles to build up their own lipid stores
and hence make the migration is similarly low (Blankenship
et al., 2006). The most logical explanation then would be
that the ovigerous females migrate to a shallower depth
and then release their brood, as proposed by Blankenship
et al. (2006). Small scale horizontal reproductive migrations
have been reported for the vent amphipod Ventiella sulfuris
Barnard and Ingram, 1990, who migrate to the periphery
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Fig. 3. A, weight to length relationship of H. gigas from 8172 m, producing a power curve equation of W = 0.0002L1.9895 (R 2 = 0.9381); B, weight to
length relationship of H. gigas from 9316 m giving a power curve equation of W = 0.00005L2.9698 (R 2 = 0.9842). (C) Displays the power curves from
8172 m (- -) and 9316 m (—) separate to the data points.
of vents to reproduce and brood (Sheader and van Dover,
2007).
The associated advantages of H. gigas spending at least
part of its life cycle at shallow depths are numerous and of
key consequence. Decreasing pressure is known to increase
the rate at which metabolic reactions proceed (Blankenship et al., 2006), therefore juveniles who mature at shallow
depths are able to assimilate food more rapidly and thus increase the rate at which they grow and become reproductive.
The higher nutritional quality and quantity of food available
at shallower parts of the trench further provides juveniles
with the opportunity to rapidly increase both their weight
and size in order to better cope with intraspecific competition and predation pressures at greater depths where H. gigas
EUSTACE ET AL.: POPULATION BIOLOGY OF HADAL AMPHIPODS
Fig. 4. Male H. gigas ( ) percentage growth between 2 and 3 was
18.68%. Female H. gigas showed a linear decrease (R 2 = 0.9998)
in percentage growth (
) as average body length ( ) increased with
developmental stage.
density is far higher. One disadvantage to such a strategy is
that in the shallower depths of the trenches (6000-8000 m),
predators such as fish and natant decapods are frequently encountered (Jamieson et al., 2009a, b, 2011). However, this
may be negated by their relatively small size and thus potentially low energy transfer with predators selectively choosing
larger prey items, and hence upon reaching notable size and
sexual maturity descend to depths where predator abundance
is low.
Female H. gigas show the opposite trend in vertical
structure to juveniles, with their presence being minimal at
shallow sites and increasing with depth towards the trench
axis (Fig. 5). This may also be related to the correlated
increase in pressure. Neither this study nor any previous
studies using baited traps have found egg-laden females
of Hirondellea, thus it appears that ovigerous females are
not attracted to carrion (Hessler et al., 1978; France, 1993;
Perrone et al., 2002; Blankenship et al., 2006). This has been
interpreted by some as a behavioural strategy by ovigerous
females to reduce the risk of embryo mortality through
Fig. 5. Percentage female (dark grey), male (hatched) and juvenile (light
grey) H. gigas. Data are combined from this study of the Izu-Bonin trench
at 8172 m (n = 647) and 9316 m (n = 717) and data from the Philippine
trench at 9604 m (n = 4127) (Hessler et al., 1978).
799
predation at feeding swarms (Hessler et al., 1978; Perrone
et al., 2002). In this instance, females may then derive their
energy from other food sources, such as detritus. However
in a study by Hessler et al. (1978) although all size classes
sampled contained some amount of sediment in the gut,
the amounts of this sediment decreased with increasing
amphipod size. This is comparable to H. dubia individuals
where, based on stable isotope analysis, Blankenship and
Levin (2007) concluded that juveniles rely on detritivory
to a greater extent than adults. An alternative explanation
therefore, is that once females become ovigerous they
stop feeding to prevent the expulsion of eggs via swelling
of their midgut (Hessler et al., 1978; Blankenship et al.,
2006). Sainte-Marie et al. (1990) noted that shallowing
of the body cavity of ovigerous females of the shallowwater lysianssoid Anonyx sarsi Steele and Brunel, 1968
resulted in severe gut constriction, and in the days preceding
oviposition the body cavity was completely filled with ova
and the lumen of the gut was closed, thus severely inhibiting
or most probably preventing feeding. If this is also the
case for H. gigas then females must undergo a period
of starvation whereby they are maintained by their lipid
reserves (Hessler et al., 1978). If brooding females remain in
the deepest parts of the trench then this may be an attempt to
survive the starvation period by decreasing their metabolism
through exposure to increasing pressure. However, this
would also suggest that the developing embryos would
suffer a decreased metabolism and the rate at which they
grow would decrease, further increasing the brooding period
and thus the starvation period, negating the advantages of
descending to greater depths.
Based on a large study of the available literature, SainteMarie (1991) concluded that in cold water (polar and coldtemperate habitats, bathyal depths and below) semelparity
in gammaridean amphipod species occurs significantly more
frequently than iteroparity. Iteroparity and semelparity in
cold water populations can be predicted by the ‘half-range
of mature female body length ratio’ (HMFBLr = (BLmax −
BLmean ):BLmean ) as defined by Sainte-Marie (1991). This
ratio ranges from 0.0110-0.3478 in semelparous populations
and from 0.1304-0.7846 in iteroparous populations (SainteMarie, 1991). Basing their conclusions on this predictor,
Perrone et al. (2002) postulated Peru-Chile populations
of Hirondellea spp. are semelparous. No fully sexually
mature females were collected either by us or Hessler et
al. (1978) and so HMFBLr could not be calculated for
either population. Sheader and Van Dover (2007) concluded
that in the iteroparous vent amphipod V. sulfuris mature
females revert back to the previous developmental stage
after brooding and begin preparation for the next cohort of
oöcytes. This ‘resting’ stage between broods in iteroparous
amphipods has also been suggested to occur in the deep
sea amphipod Eurythenes gryllus (Lichtenstein, in Mandt,
1822) (Ingram and Hessler, 1987). However there is little
evidence to support the theory that H. gigas display such
a reproductive strategy, quite the contrary. If this was the
case then elevated numbers of females with well developed
oöstegites would have been expected to be captured at
baited traps as they resume feeding during the ‘resting’
phase, however, only 1 individual with setose oöstegites was
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captured (9316 m 5). Similarly if oöstegites are lost after
brooding and females then go through a ‘resting’ phase it
would be expected that large females with no oöstegites or
small redeveloping oöstegites would be captured, which was
not the case. In light of this and past conclusions made by
Hessler et al. (1978); Sainte-Marie (1991) and Perrone et al.
(2002), semelparity would appear to be the most probable
reproductive strategy shown by this population of H. gigas.
The loose oöcytes contained within the 9316 m samples
present a conundrum. Based on log10 volumes and pigmentation they correspond to 5 and 6 oöcytes of Philippine
Trench populations of H. gigas (Hessler et al., 1978). Assuming populations of H. gigas from the Izu-Bonin trench
follow the same reproductive growth patterns as their conspecifics in the Philippine Trench, this raises the question
as to why 5 and 6 oocytes were present in large numbers
despite only a single 5 and an absence of confirmed 6 individuals present in the sample. Attempts to dissect out the
gonads of females of various life stages for comparative purposes were unsuccessful. Scavenging amphipods are known
to succumb to predation and cannibalism while in the traps
(Thurston, 1979). Indeed the predatory P. jamiesoni was collected with the 9316 m sample as were a number of damaged/predated specimens (n = 8) of large body size that
were omitted from the length/weight measurements due to
their damaged condition. While we remain sceptical that all
of the oocytes found within the samples came from these
predated animals, as this would imply that predators left the
gonads untouched in this instance, it is at this point the most
logical explanation. Alternatively, it may be possible that the
oocytes were forced out of the females due to decompression
upon retrieval of the traps to the surface, though this is unknown in the literature and it leaves their association with 6
of Hessler et al. (1978) unsolved. It is known that amphipods
can show a high degree of intra-specific reproductive variability between different populations (Johnson et al., 2001;
Sheader and van Dover, 2007) and so it may reasonably be
suggested that the oöcytes could have come from a 4 and
5, yet only one specimen of each of those stage cohorts
were sampled and so the likelihood of the oocytes having
come from either of these two individuals is also low.
Males collected from 9316 m were on average larger than
those collected from 8712 m (25.3 mm at 9316 m; 21.3 mm
at 8172 m) and also comprised some 3 individuals unlike
8172 m, inferring that there is an advantage to living at
greater depths for later stage males also. The increase in
body size with depth is not reflected in the abundance or
density of surface derived food-falls and is more likely
to be driven by other factors such as pressure and the
accumulation of organic matter towards the trench axis
(Danovaro et al., 2003; Jamieson et al., 2010).
We conclude that pressure per se does not drive the observed trends but rather an interaction between depth (pressure) and topography-influenced distribution of resources in
terms of both quality and quantity (Danovaro et al., 2003;
Jamieson et al., 2010). Juveniles are more abundant at shallower depths where a greater net quantity and higher quality of POM is present and the net total of food falls is the
highest (where competition is lowest) and pressure induced
effects on metabolism are beneficial for growth. Mature in-
dividuals are found deeper where their large body size no
longer makes them a target for predators due to low predator abundance and their metabolic rate can be reduced due to
the reassurance of high lipid stores. For both males and females this is advantageous during periods of starvation such
as occur in between food falls, but even more so for females
who are thought to undergo prolonged periods of starvation
during brooding.
ACKNOWLEDGEMENTS
This work was supported by the HADEEP project (funded by the Nippon
Foundation, Japan, and the Natural Environmental Research Council, UK).
We thank the chief scientist, captain and the crew of the RV TanseiMaru KT-09-03. We thank Dr. Toyonobu Fujii (University of Aberdeen,
UK) and Dr. Martin Solan (NOCS, UK) for their assistance at sea. We
thank Dr. K. Kita-Tsukamoto, Prof. H. Tokuyama and Prof. M. Nishida
at the Atmosphere and Ocean Research Institute, University of Tokyo,
Japan. A.J.J. and N.C.L. are funded by the MASTS pooling initiative (The
Marine Alliance for Science and Technology for Scotland) and their support
is gratefully acknowledged. MASTS is funded by the Scottish Funding
Council (grant reference HR09011) and contributing institutions.
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