JOURNAL OF PLANKTON RESEARCH
j
29
VOLUME
j
NUMBER
7
j
PAGES
641 – 654
j
2007
The fate of discarded appendicularian
houses: degradation by the copepod,
Microsetella norvegica, and other agents
MARJA KOSKI1*, EVA F. MØLLER1,2, MARIE MAAR1,3 AND ANDRE W. VISSER1
1
2
DANISH INSTITUTE FOR FISHERIES RESEARCH, KAVALERGÅRDEN 6, DK-2920 CHARLOTTENLUND, DENMARK, UNIVERSITY OF COPENHAGEN, HELSINGØRGADE
3
DK-3400 HILLERØD, DENMARK AND DEPARTMENT OF MARINE ECOLOGY, THE NATIONAL ENVIRONMENTAL RESEARCH INSTITUTE, FREDERIKSBORGVEJ 399,
51,
PO BOX
358, DK-4000 ROSKILDE,
DENMARK
*CORRESPONDING AUTHOR: [email protected]
Received February 2, 2007; accepted in principle April 12, 2007; accepted for publication May 9, 2007; published online May 18, 2007
Communicating editor: K.J. Flynn
Despite the potential importance of zooplankton in degradation of marine snow, the association of
colonising zooplankton with discarded appendicularian houses has not been investigated in northern
areas. We sampled the vertical distributions of appendicularians, houses and potential zooplankton
colonisers at two stations in the central North Sea during late summer. In addition, grazing
experiments were performed with the copepod Microsetella norvegica, which was assumed to be the
main contributor to house degradation. The results were used in (i) inverse modelling, to estimate
the factors which were significant in shaping the vertical distribution of houses and (ii) calculations
to estimate potential house degradation rates. M. Norvegica was able to feed on appendicularian
houses, with feeding rates up to 0.42 g C (g C)21 day21 (0.14 mg C ind.21 day21). The
model results suggested that the vertical distribution of houses was shaped by sinking of
houses, bacterial degradation and feeding of M. norvegica and invertebrate larvae. The estimated
community degradation rate by M. norvegica was low, whereas invertebrate larvae had degradation
rates close to bacterial degradation. We conclude that at the typical concentrations of M. norvegica
in the North Sea (104 ind. m22), its role in marine snow degradation is likely to be
small. Degradation by other zooplankton groups, such as invertebrate larvae, can, however, be
substantial.
I N T RO D U C T I O N
Marine snow may constitute a substantial source of
organic carbon in the water column (Alldredge, 1972;
Alldredge and Silver, 1988), and, together with copepod
faecal pellets, is believed to be the main vehicle of vertical material transport in the ocean (Fowler and Knauer,
1986). Marine snow forms from a number of different
types of particles, such as phytoplankton, detritus,
feeding webs, faecal material or inorganic particles,
either by physical coagulation or by zooplanktonmediated aggregation (Kiørboe, 2001). Discarded larvacean houses are the most significant zooplankton-derived
source of marine snow (Alldredge and Silver, 1988),
being an important component of the particulate
organic carbon flux both in oceanic and coastal areas
(Alldredge, 2005).
At normal salinity and temperature ranges of the
North Sea, the common appendicularian O. dioica produces 0.5– 8.2 houses ind.21 day21 (Sato et al., 2001;
Vargas et al., 2002; Tiselius et al., 2003) and may
produce and abandon more than 50 houses during its
life-time (Sato et al., 2001). These discarded houses are
rich sources of phytoplankton, bacteria, flagellates,
faecal pellets, mineral grains and other particles
(Alldredge and Silver, 1988) e.g. the concentration of
diatoms and pellets in abandoned houses can exceed
doi:10.1093/plankt/fbm046, available online at www.plankt.oxfordjournals.org
# The Author 2007. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
JOURNAL OF PLANKTON RESEARCH
j
29
VOLUME
their concentrations in ambient water, respectively, by
103 and 105 times (Hansen et al., 1996). Discarded
appendicularian houses, therefore, provide rich, benthiclike surfaces in pelagic environment (Alldredge, 1972;
Steinberg et al., 1994), being locations of elevated metabolic activity (Steinberg et al., 1997).
Discarded houses are frequently colonised by metazoans, such as harpacticoid and poecilostomatoid copepods and invertebrate larvae (Alldredge, 1972, 1975;
Ohtsuka and Kubo, 1991; Steinberg et al., 1994; Shanks
and Walters, 1997). These colonisers include the copepods Oncaea spp. and Microsetella spp., both of which
have morphology and feeding strategies suited to solid
substrates (Hicks and Coull, 1983; Huys and Boxshall,
1991) and can obtain high abundances on larvacean
houses (Steinberg et al., 1994; Green and Dagg, 1997).
These species are often many times more concentrated
on houses than in an equal volume of surrounding
water (Steinberg et al., 1994) and may in fact be dependent on benthic-like surfaces to obtain food in pelagic
environment (Koski et al., 2005). Similarly, invertebrate
larvae, such as polychaetes, nematods and gastropod,
and bivalvia veligers are frequently observed in marine
snow particles (Shanks and del Carmen, 1997) and are
believed to use marine snow both as a food source
(Bochdansky and Herndl, 1992) and as a transport
vector (Shanks and Edmondson, 1990).
Qualitative observations and measurements of pellet
production have shown that aggregate colonising copepods are also able to feed on discarded appendicularian
houses and other types of marine snow (Alldredge,
1972; Ohtsuka and Kubo, 1991; Lampitt et al., 1993;
Steinberg et al., 1997; Dilling et al., 1998). The diet of
copepods within houses includes diatoms, copepod and
crustacean parts, detritus and possibly house-mucus
itself (Steinberg, 1995). Aggregate-colonizing metazoans
can also contribute significantly to the degradation of
larvacean houses and other types of marine snow
(Steinberg et al., 1997; Kiørboe, 2000), although the
sinking rates of larvacean houses can be high, up to
120 m day21 (Hansen et al., 1996). Microsetella norvegica
can potentially degrade up to 100% of the small
,0.5 cm aggregates in the North Sea (Koski et al.,
2005), whereas in the Skagerrak the degradation rate of
appendicularian houses by M. norvegica has been estimated to 34% day21 at intermediate turbulence levels
(Maar et al., 2006). Also the correlation between the
regeneration of material within appendicularian houses
and of the presence of M. norvegica, observed in the
Skagerrak (Maar et al., 2004), and the high loss rate of
appendicularian houses observed in a nearby fjord
(Vargas et al., 2002) suggest the importance of harpacticoid copepods in degradation of houses.
j
NUMBER
7
j
PAGES
641 – 654
j
2007
Although the presence of Microsetella spp., Oncaea sp.
and invertebrate larvae in giant larvacean houses and
other types of marine snow in subtropical – tropical
areas is well documented (Alldredge, 1972, 1975;
Ohtsuka et al., 1993; Steinberg et al., 1994; Shanks and
del Carmen, 1997), their association with smaller
appendicularian houses (1 – 3 mm radius) has not been
directly shown. Similarly, although it is assumed that
M. norvegica can feed on appendicularian houses, actual
observations are missing. As appendicularian houses are
an important component of the downward carbon flux
in, e.g. North Sea (Vargas et al., 2002; Maar et al., 2004),
M. norvegica is one of the dominant copepod species
in the area (Dugas and Koslow, 1984; Nielsen and
Andersen, 2002) and invertebrate larvae can at times
reach high densities, one may hypothesise that colonisation and degradation of the houses by these zooplankters can substantially affect the biogenic flux. In the
present study, we observed the vertical distributions of
appendicularians, empty houses and potential zooplankton colonisers (M. norvegica, Oncaea sp. and invertebrate larvae) as well as performed grazing experiments
with M. norvegica and discarded houses, to estimate the
role of metazoans in the degradation of appendicularian
houses.
METHOD
Vertical profiles
The study was conducted during a cruise of R.V. Dana
(Danish Institute for Fisheries Research, DIFRES), from
26 July to 4 August 2005, in the central North Sea (for
details of the sampling area, see, e.g. Nielsen et al., 1993;
Richardson et al., 2000). The vertical distribution of
M. norvegica, appendicularians (mainly Oikopleura sp.) and
empty appendicularian houses were measured at two
stations, at station 1 (56864.380 N, 3844.60 E; water
column depth ca. 65 m) on 29th July and at station 5
(56805.200 N, 4802.320 E; water column depth ca. 60 m)
on 1st August, at 5 m depth intervals. Vertical samples
were collected with 5 L Niskin bottles connected to
a CTD-rosette. Six bottles per depth were carefully
emptied into 30 L buckets; extra care was taken not to
damage the fragile houses. Four litres of the unfiltered
sample was first counted for appendicularian houses,
by carefully pouring portions of ca. 0.2 L into large
Petri dishes and scanning the water under a binocular
microscope. After counting the houses, the whole
sample (ca. 30 L) was carefully filtered onto a 50 mm net
and preserved in 4% acid lugol (final concentration).
The abundances of M. norvegica and abundance and
642
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
size (both trunk and tail length) of Oikopleura sp. were
later analysed from these samples, using a binocular
microscope. The potential house size was estimated
from a ratio of trunk length to house radius (0.43 +
0.09) obtained from a video recording of a laboratory
cultured O. dioica (P. Tiselius, Kristineberg Marine
Biological station, Sweden), by measuring 25 individuals
for trunk length and house radius. The house volume
was calculated assuming a spherical form of houses. For
comparison, the house volume was also calculated using
a house volume to trunk length regressions according to
Alldredge (Alldredge, 2005).
Other particle-colonising copepods (Harpacticoid sp.
and Oncaea sp.) and invertebrate larvae ( polychaetes,
gastropods, bivalvia and echinoderms) were counted
from 300 – 700 L samples collected at 5 m depth intervals with a submersible pump (equipped with a 30 mm
net) employed close to the time (ca. 1 day) of the vertical sampling with Niskin bottles. Ca. 30 individuals of
each species/groups were measured from each sample
( prosome length of Oncaea sp.; total length of harpacticoids and invertebrate larvae); the body carbon was estimated based on the carbon: length regressions of
Webber and Roff (Webber and Roff, 1995) for Oncaea sp.
and Uye et al. (Uye et al., 2002) for all other species.
CTD profiles with temperature, salinity and fluorescence were recorded simultaneously with all vertical
samplings. In situ fluorescence was recalculated to chlorophyll a (Chl a) using a regression between in situ fluorescence and fluorometric measurements of water column
Chl a concentrations from selected depths sampled
during the whole cruise of nine days (r 2 ¼0.80; data not
shown).
Feeding experiments and video
observations
The feeding of M. norvegica on appendicularian houses
was measured at both stations, using faecal pellet production as an estimate for feeding. M. norvegica were collected for the experiments with deep vertical hauls of a
90 mm WP-2 net with a non-filtering codend, whereas
appendicularians were collected with surface hauls
using a 1-m ring net of 90 mm with a zip-on 30 L
Plexiglas cod end. Appendicularian houses for the
experiment were collected from the codend, using
pointed light sources and large-mouthed pipettes. The
incubations consisted of 3 – 4 replicate 0.25 L bottles,
containing 10– 20 adults or late copepodites of M. norvegica and five relatively intact appendicularian houses in
GF/F filtered seawater. Approximately similar amounts
of M. norvegica were incubated in GF/F filtered seawater
and in high concentration (.500 mg C L21) of
Thalassiosira weissflogii, as a control for minimum and
maximum pellet production, respectively. The treatments with appendicularian houses and filtered seawater control were rotated, whereas the bottles with T.
weissflogii were kept still, in order to let the algae settle
on a surface and therefore to allow for the maximum
feeding rate (Koski et al., 2005). All incubations lasted
for ca. 24 h; incubations were terminated by adding
acid lugol’s solution for ca. 4% final concentration. The
number of M. norvegica and faecal pellets were later
determined using a binocular microscope, after carefully filtering the contents of each bottle onto a 15 mm
net. Pellet volume was measured earlier in similar
incubations where M. norvegica was feeding on T. weissflogii (30 080 + 21 440 mm3; Koski et al., 2005) and converted to carbon by assuming a specific carbon content
of pellets according to Gonzalez and Smetacek
(Gonzalez and Smetacek, 1994). Pellet production rates
were converted to ingestion using a significant
regression between pellet production and ingestion (y ¼
0.07 + 9x; n ¼ 25, r 2 ¼ 0.71, P , 0.0001; both in
carbon) obtained in earlier experiments with M.
norvegica feeding on T. weissflogii (Koski et al., 2005).
Differences in pellet production between treatments
were tested for significance by using a one-way
ANOVA, followed by a Tukey HSD post hoc test for
pairwise comparisons.
In addition, adults and late copepodites of M. norvegica and discarded houses were collected for video
filming. Ca. 60 M. norvegica and eight relatively intact
houses were placed into a 0.4 L cylinder with GF/F filtered seawater and kept cool and dark until the filming
ca. 2 days later. Ca. 2 h of video was recorded from
the slowly rotating (ca. 1 rpm) 0.4 L cylinder, using a
CCD video camera (Mintron MTV-1802CB) equipped
with a 105-mm lens (Nikon Micro Nikkor 1 : 2.8) and
connected to a video cassette recorder, a time-code
generator and a monitor. Infrared illumination was
provided from behind by a light emitting diode
(LED) which was collimated through a condenser. The
number of M. norvegica residing on houses and their residence time were measured by keeping an individual
house in focus, and recording the time of arrival and
departure of M. norvegica individuals. The residence time
was based on measurements of 20 different individuals.
In addition, the settling rate of two houses was estimated by recording the time of their descent from the
top to the bottom of the cylinder (7 –8 cm). After
filming, the content of the cylinder was preserved in 4%
lugol, and the number of M. norvegica and the number
and size (radius) of the houses were estimated using a
binocular microscope. The total concentration of M.
norvegica in incubations was 126 ind. L21 and the total
643
JOURNAL OF PLANKTON RESEARCH
j
house volume at the end of the incubations was ca.
20 mm3.
Model
The measured vertical profiles of appendicularian
houses reflect a dynamic process wherein houses are
produced by living appendicularia and sink and are
degraded by bacteria, zooplankton (specifically M. norvegica, Oncaea sp. and invertebrate larvae) and other
agents. We use the principle of inverse modelling to
derive estimates of the relative rates (sinking, production, degradation and clearance) from observed profiles. A general equation describing these dynamics can
be written as
@hðzÞ
@hðzÞ
¼ paðzÞ w
bhðzÞ hðzÞðm1 mðzÞ
@t
@z
þ m2 oðzÞ þ m3 lðzÞÞ
ð1Þ
where h(z), a(z), m(z), o(z) and l(z) are the depthdependent concentrations of houses, appendicularia,
M. norvegica, Oncaea sp. and invertebrate larvae, respectively. The governing rate coefficients are: p the production rate (houses appendicularia21 day21), w the
sinking speed (m day21) and mi the clearance rates by
specific zooplankton components (L ind.21 day21). The
degradation rate of houses by bacteria and other unidentified organisms such as small zooplankton (other
than those specifically examined) is denoted by b
(day21) and is assumed constant and not depthdependent. Assuming that the vertical distribution of all
agents is in steady state, the above dynamic description
can be integrated and rewritten as
ðz
0
aðzÞdz ¼
ð
w
b z
ðhðzÞ hð0ÞÞ þ
hðzÞdz
p 0
p
ð
1 z
hðzÞðm1 mðzÞ þ m2 oðzÞ þ m3 lðzÞÞdzð2Þ
þ
p 0
A multiple regression of data from the observed profiles thus present best estimates of the parameter ratios
w/p, b/p and mk/p for k ¼ 1, 2 and 3. Having an estimate of any one or other of these parameters will allow
an estimation of all the others. The multiple regressions
are performed in SPSS (ver.11.5). The specific model
that is tested is
IAi ¼ C0 þ C1 Hi þ C2 IHi þ C3 IHMi
þ C4 IHOi þ C5 IHLi
29
VOLUME
ð3Þ
j
NUMBER
7
j
PAGES
641 – 654
j
2007
where IAi and IHi are the appendicularian and house
concentrations, respectively, integrated from the surface
to depth zi, Hi is h(zi) – h(surface). IHMi, IHOi and IHLi
are the integrated product of house and M. norvegica
(copepodites and nauplii), Oncaea sp. and invertebrate
larvae concentrations from the surface to depth zi. A
backward, stepwise regression (SPSS ver.11.5) was used
to determine the combination of variables that best
describe the observed distribution of appendicularian
houses. It should be noted that the underlying analysis
only detects correlations between the spatial distributions of variables. Provided such structures exist, coefficients can be determined. However, a null correlation
does not necessary imply that there is no interaction,
but can simply be due to a uniform distribution.
R E S U LT S
Study area
Both stations had a surface temperature of ca. 158C
and surface salinity close to 35‰, although the
thermo/halocline at station 5 ( just below 20 m) was
shallower and steeper than at station 1 (.30 m).
Similarly, the deep chlorophyll maximum (DCM) was
deeper (ca. 40 m) at station 1, with three times higher
maximum Chl a values of ca. 3 mg L21, compared to
ca. 1 mg L21 at station 5 (Fig. 1).
Vertical distribution and house volume
Microsetella norvegica was most abundant below the
thermocline, in or just below the DCM, whereas the
majority of appendicularians were in the surface layer
(Fig. 2). Similar to the appendicularians, peak abundance of houses (up to 6 L21) was generally observed at
20 m (Fig. 2b). The average trunk lengths were
330 + 200 mm at the station 1 and 310 + 210 mm at
the station 5. The average house volumes at stations 1
and 5 were estimated by us to be, respectively, 13 + 4
and 17 + 11 mm3, whereas the trunk length to house
volume regressions according to Alldredge (Alldredge,
2005) produced approximately two times larger average
house volumes (25 and 30 mm3 at stations 1 and 5,
respectively). The total depth integrated concentration
of M. norvegica was 34 300 and 9300 and ind. m22 at
stations 1 and 5, respectively. Other particle colonising
copepods, Oncaea sp. and harpacticoid sp. were rarer,
with maximum concentrations 2300 ind. m22, with
peak abundance of Oncaea sp. just above the thermocline and peak abundance of harpacticoids near to the
bottom. Invertebrate larvae were extremely abundant at
644
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
presence of T. weissflogii (2.1 pellets ind.21 day21; Tukey
HSD; P , 0.05) and intermediate pellet production on
appendicularian houses (0.8 – 1.4 pellets ind.21 day21;
Table I). The corresponding consumption of appendicularian houses was 0.11– 0.14 mg C ind.21 day21,
0.33 – 0.42 g C (g C)21 day21, assuming an average
size of M. norvegica to be 0.4 mg C ind.21 (Uye et al.,
2002). This was not significantly lower than ingestion of
T. weissflogii (0.52 g C (g C)21 day21 or 0.17 mg C
ind.21 day21; Tukey HSD; P .0.05).
Visual observations confirmed the feeding of M. norvegica upon empty appendicularian houses (Fig. 3).
During most of the time, the observed houses had 1 – 5
M. norvegica individuals either residing on the surface of
the house or swimming in, on and around it. With the
average density of 2.5 individuals per house, total house
volume of ca. 20 mm2 and M. norvegica density of
126 L21, M. norvegica appeared to be .800 times more
concentrated on the appendicularian houses than in the
surrounding water, with ca. 16% of the animals
attached to houses at any one instant. However, M. norvegica individuals seemed to be swimming actively
around, hopping in and out of houses at short time
intervals. This led to a relatively short residence time of
2.2 + 1.8 min (ranging between 0.2 and 6.8 min) on
the houses. The sinking velocity of the houses measured
from the video observations was 135 + 15 m day21
(n ¼ 2).
Model
Fig. 1. Vertical distribution of temperature (8C), salinity (‰)
and Chl a (mg L21) at stations 1 (closed circles) and 5 (open circles).
station 5, with a peak abundance of ca. 120 ind. L21
(99% gastropod larvae) at 35 m. At station 1, the vertical distribution of larvae was rather uniform, with a
smaller peak (12 ind. L21) dominated by echinoderms
at 15 m (Fig. 2a).
A multiple regression based on the dynamics described
in equation (3) was fit to observations. At station 1, two
coefficients are significant: C1 ¼ w/p ¼ 5.1 + 1.2 m
and C2 ¼ b/p ¼ 0.38 + 0.10, suggesting that the
observed vertical distributions are primarily controlled
by three processes: house production, sinking of houses
and degradation by bacteria and other unidentified
organisms. Ingestion by Oncaea sp. was of marginal significance (C4 ¼ 4 + 2), whereas grazing by M. norvegica
and invertebrate larvae were not significant (P . 0.05).
At station 5, the significant coefficients were C2 ¼ b/
p ¼ 0.27 + 0.01, C3 ¼ m/p ¼ 0.5 + 0.2 and C5 ¼ m/
p ¼ 0.007 + 0.001, suggesting an effect of house production, degradation by bacteria and degradation by
M. norvegica and invertebrate larvae (Table II).
Feeding and behaviour
The pellet production of M. norvegica was significantly
different between treatments (one-way ANOVA; F3 ¼
6.2, P , 0.05), with very low pellet production of individuals kept in filtered seawater (0.03 pellets ind.21
day21), significantly higher pellet production in the
DISCUSSION
We used two approaches to estimate the potential
importance of different zooplankton colonisers for house
degradation. First, an inverse model was constructed to
645
JOURNAL OF PLANKTON RESEARCH
j
VOLUME
29
j
NUMBER
7
j
PAGES
641 – 654
j
2007
Fig. 2. Vertical distribution of (A) M. norvegica nauplii, copepodites, other harpacticoids and Oncaea sp. and invertebrate larvae (ind. L21) and
(B) appendicularians, discarded appendicularian houses (no L21) and average (+SD) house volume at stations 1 (closed symbols; straight line)
and 5 (open symbols; dotted line). Note different scales of the x-axis.
646
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
Table I: Pellet production and corresponding rates. A combination of the calculated rates and model
predictions of significance should therefore give an idea
ingestion of M. norvegica
Treatment
Houses,
station 1
Houses,
station 5
Fw
T. weissflogii
Pellet production
Ingestion
Pellets ind.21
day21
g C (g C)21
day21
mg C ind.21
day21
g C (g C)21
day21
0.8 + 0.2
0.003
0.11
0.33
1.4 + 0.5
0.006
0.14
0.42
0.03 + 0.02
2.1 + 0.3
0.0001
0.009
0.07
0.17
0.22
0.52
of which of the investigated groups can potentially be
significant for shaping the vertical profiles of the houses
and what magnitude of degradation rates can roughly
be expected. These two approaches, their shortcomings
and the estimated impact of different processes for vertical distribution of appendicularian houses in the study
area are discussed below.
Pellet production (in pellets ind.21 day21 and as g C (g C)21 day21;
mean + SE) and corresponding ingestion (mg C ind.21 day21 and g C (g
C)21 day21; see Methods) of M. norvegica adults and late copepodites
on discarded appendicularian houses (stations 1 and 5), in GF/F filtered
seawater (FW) and in high concentration of the diatom T. weissflogii. The
pellet production and ingestion in filtered seawater represent the
background pellet production due to, e.g. previous feeding.
evaluate which factors were significant in shaping the
vertical distribution of the houses. The limitation of the
model is that it only detects significance if there are vertical structures, whereas a uniform distribution will
never appear significant in the model (cf. vertical distribution of invertebrate larvae at station 1). Secondly, the
population grazing rates and their percentage from the
house biomass were calculated based on the observed
vertical distributions and either measured grazing rates
(M. norvegica) or weight-specific grazing rates reported in
literature. Although the obtained population grazing
rates include several uncertainties, they should nevertheless give a rough estimate of the potential degradation
Fig. 3. Microsetella norvegica feeding on discarded appendicularian
houses ( photo from the video recording). The arrows indicate M.
norvegica individuals. The average prosome length of M. norvegica is ca.
0.5 mm.
Significant factors affecting the vertical
profiles of houses – the model results
The inverse model suggested a significant role of house
production, sinking of houses and degradation by bacteria (and other unidentified organisms) at station 1,
and house production, degradation by bacteria and
degradation of M. norvegica and invertebrate larvae at
station 5. In addition, degradation of Oncaea sp. was
marginally significant at station 1 (Table II).
The coefficient C1 (5.1; Table II) describes the ratio
of house sinking to house production (w/p) and is not
dimensionless (it has dimensions [m]). This means that
over the period that an appendicularian sheds a house,
one such discarded house will have sunk about 5 m. The
sinking velocity of houses can then be estimated to ca.
40 m day21, assuming a production of 8 houses ind21
day21 at 158C (Sato et al., 2001). This rate is very similar
to that estimated from the house volume according to
Alldredge and Gotschalk (Alldredge and Gotschalk,
1988), 33– 41 m day21, and in the same order of magnitude as suggested by Hansen et al. (Hansen et al., 1996)
for O. dioica houses (120 m day21) or as measured from
the video observations (135 + 15 m day21). Why the
sinking of houses was significant at station 1 but not at
station 5 is not clear: if the sinking rate is estimated by
calculations based upon the house volume (Alldredge
and Gotschalk, 1988), the average sinking rate at station
5 (41 + 11 m day21) was higher than at station 1 (33 +
7 m day21). As marine snow tends to accumulate in or
above density discontinuity layers (Alldredge and
Youngbluth, 1985), differences in the shape and placing
of the pycnocline at the two stations (Fig. 1) could have
affected the settling velocities.
Degradation by bacteria and other unidentified
organisms (coefficient C2) was significant for shaping
the vertical distributions of discarded houses both at
stations 1 and station 5, with, respectively, 38 and 27 %
of the produced houses being degraded daily (Table II).
Specifically, assuming P ¼ 8 houses appendicularian21
day21, community degradation was b ¼ 3 houses day21
at station 1 and slightly lower at b ¼ 2 houses day21 at
station 5. Since bacterial degradation of aggregates has
647
JOURNAL OF PLANKTON RESEARCH
j
29
VOLUME
j
NUMBER
7
j
PAGES
641 – 654
j
2007
Table II: Multiple regression coefficients and their significance for the model described in equation (3)
Station 1
N ¼ 12
Rsqr ¼ 0.975
Adj Rsqr ¼ 0.966
Station 5
N ¼ 10
Rsqr ¼ 0.999
Adj Rsqr ¼ 0.999
C0
C1
C2
C3
C4
C5
C0
C1
C2
C3
C4
C5
Coefficient
SE
F-to-remove
8.891
5.094
0.377
—
4.045
—
0.180
—
0.271
0.526
—
0.00714
3.129
1.151
0.104
—
1.833
—
0.396
—
0.0115
0.198
—
0.00131
—
19.6
7.3
—
4.9
—
—
—
560
7.1
—
30
F-to-enter
—
—
—
0.007
—
0.43
—
0.78
—
—
0.49
—
P
0.002*
0.027*
0.965
0.058
0.532
0.406
,0.001*
0.032*
0.508
,0.001*
Multiple regression coefficients and their significance for the model described in Eq (3) and fitted to observations at the two different stations. Values
reported are for the best fit from a backward stepwise regression. P , 0.05 are deemed to be significant (marked with *). C1 describes the ratio of
house sinking to house production (w/p), C2 the bacterial degradation (b/p) and C3, C4 and C5 characterise the clearance by M. norvegica, Oncaea sp.
and invertebrate larvae, respectively. For further explanation, see the text.
previously estimated to be ca. 8% of the aggregate
carbon day21 (Plough and Grossart, 2000), a degradation
rate between 0.3 and 0.4 day21 seems to be relatively
high and therefore most likely includes house degradation by organisms other than bacteria. Apart from
bacteria and zooplankton groups considered here possible candidates for organisms feeding on appendicularian houses could be the heterotrophic dinoflagellate
Noctiluca spp. (Tiselius and Kiørboe, 1998), calanoid and
cyclopoid copepods (Ohtsuka et al., 1993; Dilling et al.,
1998) or crustacean nauplii (Steinberg et al., 1994), all of
which have been observed in marine snow particles and
are assumed at least occasionally to consume marine
snow (Kiørboe, 2000).
Other than bacterial degradation, grazing by M. norvegica and invertebrate larvae appeared to be contributing to the observed profile at station 5 (C3 and C5,
respectively), whereas the clearance by Oncaea sp. was of
marginal significance at station 1 (C4). The coefficient
of 0.5 for M. norvegica clearance (Table II) implies that
during the time that it takes an appendicularian to
produce one house, M. norvegica will clear aggregates
from ca. 0.5 L of water. Assuming a house production
of 8 day21 (see above), this would imply a clearance
rate of ca. 4 L ind.21 day21. This is in the same order
of magnitude as the search volume suggested for 0.1 cm
radius aggregates by Kiørboe (Kiørboe, 2000) or as
calculated for locating sinking appendicularian houses
of 0.2 cm by Maar et al. (Maar et al., 2006), indicating
that it is realistic to assume that a M. norvegica individual
could search 4 L of water for aggregates day21,
although an actual clearance rate of 4 L ind.21 day21 is
too high. Similarly, the coefficient of 4 for Oncaea sp.
clearance is unrealistically high, but a realistic clearance
rate of Oncaea sp. would likely be ,100 mL ind.21
day21, as measured by Paffenhöfer for Oncaea mediterranea (Paffenhöfer, 1993). A realistic volume for clearance
rate for M. norvegica is difficult to estimate, because
this species is inefficient in feeding from suspension
(Koski et al., 2005), but, assuming an ingestion rate of
100% body weight21 day21 and the present house
concentration in the vertical peak abundance of
M. norvegica, ,100 mL ind.21 day21 would be in a realistic range. Therefore, the clearance rate coefficients for
M. norvegica and Oncaea sp. are overestimated, and
should only be taken as an indication that these species
can potentially be important as a grazer of appendicularian houses. The substantially lower coefficient of
0.007 for invertebrate larvae (0.06 L ind.21 day21)
appears as a more realistic estimate, and probably
reflects the generally lower swimming abilities and
smaller size (leading to lower ingestion rates) of invertebrate larvae. If calculated as an ingestion rate, 0.06 L
ind.21 day21 would, at the peak depth of invertebrate
larvae (e.g. 35 m at station 5), imply an ingestion of
ca. 0.05 houses ind.21 day21, corresponding to ca.
0.35 mg C ind.21 day21. This is very close to the rates
estimated for, e.g. polychaete larvae (Bochdansky and
Herndl, 1992).
The two stations were, however, different with respect
to the groups contributing to the degradation rates.
With Oncaea sp., the marginal significance at station 1
was probably due to a .2 times higher density at this
station, since at both stations the vertical distribution of
Oncaea sp. was similar. Similarly, the peak abundance of
invertebrate larvae at station 5 was extremely high (ca.
120 ind. L21), compared with the rather uniform distribution of larvae at station 1 (always ,13 ind. L21).
However, if the potential grazing impact of larvae was
calculated per surface area (see below), there was no
648
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
clear difference between the two stations (Fig. 4). It
appears likely that the lack of significance of invertebrate larvae at station 1 is rather a follow-up of the
model limitations in recognising factors with uniform
vertical distribution than a reliable result suggesting a
real difference between the two stations. In contrast,
although the abundance of M. norvegica was higher at
station 1 where no significant effect was detected, the
vertical distributions at the two stations were different,
as were the feeding rates (with a higher feeding rate at
the station 5; Table I). The significance of M. norvegica
feeding at station 5 but not station 1 was therefore likely
a combination of the differences in vertical distribution
and feeding rate between the stations.
Fig. 4. Potential consumption of discarded appendicularian houses
by particle colonizing copepods (M. norvegica, harpacticoida sp. and
Oncaea spp.) and invertebrate larvae as a percentage of the observed
houses (day21) at stations 1 and 5. For parameters used to estimate
population grazing rates, see Table IV, for explanations of minimum
and maximum estimates, see Discussion.
Potential population grazing rates:
calculations based on vertical profiles
and feeding rates
In addition to bacterial degradation rates, the model
results suggested a potential importance of invertebrate
larvae, M. norvegica and possibly also Oncaea sp. in
shaping the vertical distribution of the houses. Here we
attempt to estimate the potential population grazing
rates of these organisms and their proportion of the
observed house biomass and estimated house production rates.
The grazing rate of M. norvegica on appendicularian
houses was measured based on pellet production.
Although the pellet production of M. norvegica was low, it
was considerably higher than in filtered seawater, and
thus indicated ingestion of house material during the
incubations. Using the pellet production as a quantitative estimate of feeding is, however, problematic.
Besides the problems connected to the effects of, e.g.
food quality on pellet production (Besiktepe and Dam,
2002), the faecal pellets produced by M. norvegica are
small, and are thus likely to disintegrate fast. In previous
experiments, where ingestion and pellet production of
M. norvegica were measured simultaneously (Koski et al.,
2005), the number of faecal pellets was unrealistically
low, most likely due to the disintegration of the pellets
during the 24-h incubations. The pellet production of
M. norvegica in incubations should therefore be considered as a conservative minimum estimate of the
pellet production on appendicularian houses.
The regression used to convert pellet production to
ingestion originated from exactly the same type of incubations as used in the present experiments and thus
included the effect of disintegrating pellets (Koski et al.,
2005). Assuming that the amount of disintegrating
pellets was similar in the present experiments, the calculated ingestion rates should therefore represent the
actual feeding rates better than the measured pellet
production rate. If the effect of previous feeding ( pellet
production in filtered seawater) was extracted from the
ingestion on appendicularian houses, the ingestion rate
of M. norvegica was 0.04 – 0.07 mg C ind.21 day21, which
corresponded to 11– 20% of the body weight per day.
This estimate is rather similar to most estimates of zooplankton feeding on marine snow (mostly 40% body
weight; Table III), and supposedly sufficient to support
the generally low growth rate of M. norvegica in corresponding temperatures (Uye et al., 2002).
However, the concentration of houses in feeding
incubations was ca. 3 times higher than the observed
peak concentrations in the water column during the
study. If we assume that ingestion only depends on
649
Estimated ingestion/carbon demand
Species
A
Individual mg C ind.
(% body C day21)
a
2.8 (40)
0.04 –0.07 (11 –20)
0.4 – 2.2 (20 –100)
7 –43 (8 – 48)b
226 –271 (4 – 6)
9.6 (2)
1.7 (24)
25 –47 (2 –5)c
Polychaete larvae (Prionospio sp.)
Zooplankton
Algae
Diverse; 0.1 cm radius
Respiration
Abundance, metabolic rates
0.09 –0.22 (14 –34)
Reference
14– 960 m
220/460 m22
290 –7790 m22
18– 91
0.1
90– 400 m22
40 house21
22– 42 000 m22 (1987)
3–6000 m22 (1988)
0.06–2
6
5–58 (1987)
1–9 (1988)
2–5
19– 67
Alldredge, 1972
This study
Koski et al., 2005
Dilling et al., 1998
Dilling et al., 1998
Lampitt et al., 1993
Steinberg et al., 1997
Dagg, 1993
0.48 aggregate21
Bochdansky and Herndl, 1992
Kiørboe, 2000
7
j
PAGES
641 – 654
(A) Incubations, (B) in situ measurements and (C) theoretical calculations. If not given in the paper, the pellet production rates were converted to ingestion by using an assimilation efficiency of 60% as
suggested by Steinberg et al. (Steinberg et al., 1997), the carbon content of pellets was estimated based on a carbon to volume ratio according to Gonzalez and Smetacek (Gonzalez and Smetacek, 1994),
the carbon content of pellets and marine snow were assumed to be, respectively, 40 and 20% from the dry weight (Alldredge, 1979) and the carbon content of organisms was assumed to be 5.2% of
the wet weight (Mullin, 1969). If not given directly in the paper, the population grazing rates and potential degradation were, as far as possible, calculated from the data given in the paper.
a
Assuming a pellet size of 250 73 mm (Beaumont et al., 2002), body size of ca. 1 mm, and length to weight ratio according to Webber and Roff (Webber and Roff, 1995).
b
Assuming a body carbon of ca. 90 mg ind.21 (Vidal, 1980).
c
Assuming a body carbon of ca. 1000 mg ind.21 as suggested in the paper.
NUMBER
Pellet production
Pellet production
Pellet production
Pellet production
Ingestion
Pellet production
Community respiration
Gut chlorophyll
% day21
23
j
Houses
Houses
Artificial, diatoms
Houses, diatoms
Houses, diatoms
Diverse
Houses
Unknown
Community mg C day21
29
Oncaea mediterranea
M. norvegica
Harpacticoids (Amonardia normanni)
Calanus pacificus
Euphasia pacifica
Amphipods (Themisto compressa)
Community (Oncaea sp.)
Neocalanus cristatus
day
VOLUME
C
Original measurement
Degradation
21
j
650
B
Snow type
21
JOURNAL OF PLANKTON RESEARCH
Table III: Summary of the literature data on ingestion and degradation of marine snow by metazoans
j
2007
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
encounter rate of houses (Kiørboe, 2000) and that residence times and feeding rates are thus constant, the
actual ingestion rate of M. norvegica in the study area
would be 0.01 – 0.02 mg C ind.21 day21. The total
depth-integrated ingestion of M. norvegica would then be
ca. 460 and 220 mg C m22 day21 at stations 1 and 5,
respectively; corresponding to 0.1% of the
depth-integrated biomass of appendicularian houses
(Table IV). The assumptions of the high importance of
M. norvegica for degradation of marine snow are mostly
based on the observations of their high abundance in
aggregates (e.g. Green and Dagg, 1997), whereas quantitative grazing rates on any types of aggregates have
never been measured. If 0.02 mg C ind.21 day21 is
taken as a representative grazing rate on appendicularian houses at the concentration comparable to the
present study (131 000 houses m22, or 6 houses
L21 at the depth of the peak abundance) a M. norvegica
concentration needed for a substantial degradation rate
of houses (e.g. 10%) would need to be close to 106
ind. m22. This is consistent with the model suggestions
of Koski et al. (Koski et al., 2005), showing substantial
fractional degradation rates of M. norvegica on aggregates
of 0.1– 0.2 cm (radius) only at concentrations between
105 and 106 ind. m22. Although high densities of M.
norvegica are not uncommon (Daro, 1988), many of the
previous observations in the North Sea and nearby
fjord areas suggest M. norvegica abundances around 104
ind. m22 (Maar et al., 2004; Titelman and Fiksen, 2004;
Koski et al., 2005), as also observed in the present study.
It seems therefore that although M. norvegica is likely to
feed on aggregates and might be a significant factor in
shaping their vertical distribution, typical North Sea
concentrations are too low for substantial degradation
rates to occur and the impact of M. norvegica on the
degradation of marine snow should thus not be
overemphasised.
To estimate the potential population grazing rates of
other investigated species and/or groups (Oncaea sp.,
harpacticoid sp. and invertebrate larvae), we used
aggregate grazing rates available in literature. Where
possible, these were converted to carbon-specific rates
(Table III). As most studies estimating the ingestion
rates on marine snow were done in laboratory with relatively high concentrations of aggregates, they are likely
to overestimate ingestion in natural aggregate concentrations: assuming that the ingestion rate depends
mainly on encounter rate (Kiørboe, 2000), the high
aggregate concentrations in incubations result in higher
encounter and ingestion rates than would be observed
at the house concentrations corresponding to the present
study. Therefore, we estimated both maximum and
Table IV: Potential impact of zooplankton on house degradation and the parameters used to calculate it
Size
Species
Station 1 (0 –55 m)
M. norvegica
Oncaea spp.
Harpacticoida spp.
Polychaeta spp.
Gastropoda spp.
Bivalvia spp.
Echinodermata spp.
Total
Station 5 (5 –50 m)
M. norvegica
Oncaea spp.
Harpacticoida spp.
Polychaeta spp.
Gastropoda spp.
Bivalvia spp.
Echinodermata spp.
Total
Maximum feeding rate
Potential impact
Length
(mm)
Carbon
(mg C
ind.21)
Individual
(mg C
(ind)21
day21)
Population
min./max.
(mg C m22)
Biomass
min./max.
(% m22)
Production
min./max.
(% m22)
34.3
2.3
0.9
19.6
33.4
58.0
132.0
281
407 + 6
281 + 5
548 + 24
478 + 21
249 + 10
285 + 9
704 + 27
0.33
0.49
0.58
0.4
0.1
0.2
0.9
0.01
0.20
0.58
0.54
0.03
0.04
0.23
456
32/456
31/526
590/10 560
49/1003
122/2320
2760/30 350
4040/45 670
0.1
0.01/0.1
0.01/0.1
0.2/3.0
0.01/0.3
0.03/0.7
0.8/8.5
1.1/13
0.03
0.002/0.03
0.002/0.03
0.03/0.6
0.003/0.06
0.007/0.1
0.2/1.8
0.2/2.7
9.3
1.3
0.8
16.8
1203
20.6
6.7
1260
407 + 6
291 + 9
423 + 33
585 + 29
166 + 6
218 + 9
604 + 25
0.33
0.53
0.35
0.7
0.06
0.1
0.7
0.02
0.21
0.35
0.36
0.01
0.02
0.17
217
53/267
16/283
1060/6040
2244/12 030
76/412
198/1130
3960/20 380
0.04
0.01/0.05
0.003/0.05
0.2/1.1
0.4/2.2
0.01/0.08
0.04/0.2
0.7/3.7
0.02
0.004/0.02
0.001/0.02
0.08/0.4
0.2/0.9
0.005/0.03
0.01/0.08
0.3/1.5
Abundance
(103 m22)
8 Depth integrated grazing rate (mg C m22) and potential impact (% day21) of different zooplankton groups on degradation of discarded houses and the
parameters used to calculate it. For M. norvegica the weight-specific feeding rates were corrected for the lower in situ house numbers (see
Discussion) and multiplied by the depth-integrated abundance. For other species/groups, both minimum and maximum grazing rates were calculated
(see Discussion), using weight-specific grazing rates from literature (see Table III). Weight-specific ingestion of gastropod, bivalvia and echinodermata
larvae was assumed to be similar to weight-specific ingestion of polychaete larvae.
651
JOURNAL OF PLANKTON RESEARCH
j
29
VOLUME
minimum population grazing rates. For maximum estimates, we simply used the reported weight-specific
ingestion rates from the literature (Table III) and the
observed number of animals in the water column,
assuming that all the individuals would be sitting in the
aggregates. For minimum estimates, we first calculated
the number of individuals per aggregate, based on
aggregate volume and number of individuals in the
water column, according to Kiørboe (Kiørboe, 2000)
and multiplied this with the weight-specific grazing
rates. As it is likely that the residence times of animals
on aggregates are relatively short (e.g. 2.2 min for
M. norvegica), but the gut is filled fast during these short
visits, the actual short-term ingestion rates may be
much higher than the 24-h average (Koski et al., 2005)
and using the corrected numbers of individuals per
aggregate together with the 24-h ingestion rates will
result in a conservative minimum estimate for community grazing rates. For instance, using the maximum
feeding rates of M. norvegica from incubations (0.04–
0.07 mg C ind.21 day21) and an abundance on aggregates estimated based on the regressions in Kiørboe
(Kiørboe, 2000) resulted in 10– 20 times lower community grazing rates (17 and 11 mg C m22 day21 at
stations 1 and 5, respectively) than using the grazing
rates estimated in incubations and corrected for the
house density and the observed M. norvegica abundance.
The real community degradation rates are thus somewhere between these two estimates.
Using these two calculations, the range of
depth-integrated ingestion rates of particle colonising
copepods (M. norvegica, Oncaea sp. and harpacticoida sp.)
would be 520 – 1438 mg C m22 day21 at station 1 and
290– 770 mg C m22 day21 at station 5. The total
depth-integrated ingestion of invertebrate larvae would
be 6 – 12 times higher; namely 3520 – 44 240 and
3580– 19 610 mg C m22 day21 at stations 1 and 5,
respectively, and the total depth-integrated ingestion of
all potentially colonising zooplankton groups, respectively, 4040 – 45 670 and 3960– 20 380 mg C m22 day21.
If calculated per house, the range of zooplankton
grazing would be 0.05 – 0.5 mg C house21 day21 at
station 1 and 0.03 –0.2 mg C house day21 at station
5. These rates were rather comparable to the few rates
presented in literature, with majority of the estimated
community grazing rates being ,104 mg C m22
(Table III). The maximum house-specific rates were, in
addition, very close to the estimate of 0.48 mg C day21
for aggregates of comparable size (0.1 cm radius) presented in Kiørboe (Kiørboe, 2000).
Assuming a house volume to carbon ratio as in
Alldredge (Alldredge, 1998), the percentage of the zooplankton grazing from house biomass is between 1 and
j
NUMBER
7
j
PAGES
641 – 654
j
2007
13% day21 at station 1 and ,4% day21 at station 5
(Table IV), which is comparable to the few previous
estimates with copepods and polychaete larvae
(Table III). If the potential house production is considered (Sato et al., 2001), the impact of zooplankton at
stations 1 and 5 is, respectively, ,3% day21 and ,2%
day21. Although these rates appear low, they are rather
similar to the estimated rates for bacterial remineralisation of aggregates (8% day21; Plough and Grossart,
2000). Further, the grazing impact varies with depth:
although copepod impact is low (,3% day21), irrespective of the calculation method or depth, grazing by
invertebrate larvae could at its maximum consume 20–
30% of the appendicularian house biomass at their
peak distribution (Fig. 4). If the sinking rate of the
houses are assumed to be between 30 and 40 m day21
(see above), using the maximum population grazing
rates between 20 and 30% of the house carbon would
be degraded by zooplankton during its decent to the
bottom.
In summary, our results demonstrate feeding of
M. norvegica on discarded appendicularian houses and
suggest that particle colonising copepods and invertebrate larvae can potentially influence the vertical profiles of O. dioica house biomass. However, at typical
M. norvegica and Oncaea sp. concentrations in the North
Sea, the degradation rate due to copepod activity is
likely to be low. Thus, although M. norvegica and other
colonising copepods are probably dependent on aggregate carbon, the aggregate degradation rates do not
often seem to be dependent on copepods. It should be
noted, however, that as the ingestion rates of Oncaea sp.
and harpacticoid sp. are relatively high (Table IV),
small increases in their abundance can probably
substantially increase their contribution to house
degradation. Invertebrate larvae appear as more
important contributors to the house degradation, with
maximum degradation rates close to bacterial degradation. Therefore, zooplankton do not appear unimportant in degradation of appendicularian houses, although
it should be acknowledged that for small species such
as M. norvegica to have a substantial role, their concentrations need to be high. Our study suggests that in
late summer at the North Sea roughly up to 30% of the
discarded appendicularian houses can be degraded due
to zooplankton activities during their decent to
the bottom. However, both more accurate grazing rates
of different zooplankton species on different types of
marine snow and a seasonal sampling of colonising
zooplankton and aggregate biomass are needed before
anything further can be said about the annual importance of zooplankton on degradation of marine snow in
the area.
652
M. KOSKI ET AL.
j
DEGRADATION OF APPENDICULARIAN HOUSES
AC K N OW L E D G E M E N T S
We would like to thank T.G. Nielsen for providing the
appendicularian net, P. Tiselius for the video recordings
of Oikopleura dioica, S. Jónasdóttir (SNF-21-03-0487) for
the phytoplankton counts, H. Parner for the Chl a and
T. Kiørboe for the constructive criticism on the previous
version of the manuscript. M.K. and E.F.M. were
financed by the Carlsberg Foundation and M.A.M by
the Danish Research Agency project CONWOY
(SNF-2052-01-0034).
Dilling, L., Wilson, J., Steinberg, D. and Alldredge, A. (1998) Feeding
by the euphausiid Euphasia pacifica and the copepod Calanus pacificus
on marine snow. Mar. Ecol. Prog. Ser., 170, 189– 201.
Dugas, J. C. and Koslow, J. A. (1984) Microsetella norvegica: a rare report
of a potentially abundant copepod on the Scotian Shelf. Mar. Biol.,
84, 131– 134.
Fowler, S. W. and Knauer, G. A. (1986) Role of large particles in the
transport of elements and organic compounds through the ocean
water column. Prog. Oceanogr., 16, 147–194.
Green, E. P. and Dagg, M. J. (1997) Mesozooplankton association
with medium to large marine snow aggregates in the northern Gulf
of Mexico. J. Plankton Res., 19, 435– 447.
Gonzalez, H. E. and Smetacek, V. (1994) The possible role of cyclopoid copepod Oithona in retarding vertical flux of zooplankton
faecal material. Mar. Ecol. Prog. Ser., 113, 233–246.
REFERENCES
Alldredge, A. L. (1972) Abandoned larvacean houses: a unique food
source in the pelagic environment. Science, 177, 885– 887.
Alldredge, A. L. (1975) Discarded appendicularian houses as sources
of food, surface habitats, and particulate organic matter in planktonic environments. Limnol. Oceanogr., 21, 1 –23.
Alldredge, A. L. (1979) The chemical composition of macroscopic
aggregates in two neritic seas. Limnol. Oceanogr., 24, 855– 866.
Alldredge, A. L. (1998) The carbon, nitrogen and mass content of
marine snow as a function of aggregate size. Deep-Sea Res. I., 45,
529–541.
Alldredge, A. L. (2005) The contribution of discarded appendicularian
houses to the flux of particulate organic carbon from oceanic
surface waters. In Gorsky, G., Youngbluth, M. J. and Deibel, D.
(eds), Response of Marine Ecosystems to Global Change. Contemporary
Publishing International, Paris, France, 309– 326.
Hansen, J. L. S., Kiørboe, T. and Alldredge, A. L. (1996) Marine
snow derived from abandoned larvacean houses: sinking rates, particle content and mechanisms of aggregate formation. Mar. Ecol.
Prog. Ser., 141, 205– 215.
Hicks, G. R. F. and Coull, B. C. (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanogr. Mar. Biol. Ann. Rev., 21,
67– 175.
Huys, R. and Boxshall, G. A. (1991) Copepod Evolution. Ray Soc. Nat.
Hist. Mus., London.
Kiørboe, T. (2000) Colonisation of marine snow aggregates by invertebrate zooplankton: abundance, scaling, and possible role. Limnol.
Oceanogr., 45, 479– 484.
Kiørboe, T. (2001) Formation and fate of marine snow: small-scale
processes with large-scale implications. Sci. Mar., 65, 57–71.
Koski, M., Kiørboe, T. and Takahashi, K. (2005) Benthic life in the
pelagial: aggregate encounter and degradation rates by pelagic harpacticoid copepods. Limnol. Oceanogr., 50, 1254– 1263.
Alldredge, A. L. and Youngbluth, M. J. (1985) The significance of
macroscopic aggregates (marine snow) as sites for heterotrophic
bacterial production in the mesopelagic zone of the subtropical
Atlantic. Deep-Sea Res., 32, 1445–1456.
Lampitt, R. S., Wishner, K. F. and Turley, C. M. et al. (1993) Marine
snow studies in the Northeast Atlantic Ocean: distribution, composition and role as a food source for migrating plankton. Mar. Biol.,
116, 689– 702.
Alldredge, A. L. and Gotschalk, C. C. (1988) Direct observations of the
mass flocculation of diatom blooms: characteristics, settling velocities
and formation of diatom aggregates. Deep-Sea Res., 36, 159– 171.
Maar, M., Nielsen, T. G., Gooding, S. et al. (2004) Trophodynamic
function of copepods, appendicularians and protozooplankton in
the late summer zooplankton community in the Skagerrak. Mar.
Biol., 144, 917– 933.
Alldredge, A. L. and Silver, M. W. (1988) In situ settling behaviour of
marine snow. Limnol. Oceanogr., 33, 339– 351.
Beaumont, K. L., Nash, G. V. and Davidson, A. T. (2002)
Ultrastructure, morphology and flux of microzooplankton faecal
pellets in an East Antarctic fjord. Mar. Ecol. Prog. Ser., 245,
133–148.
Besiktepe, S. and Dam, H. G. (2002) Coupling of ingestion and defecation as a function of diet in the calanoid copepod Acartia tonsa.
Mar. Ecol. Prog. Ser., 229, 151– 164.
Bochdansky, A. B. and Herndl, G. J. (1992) Ecology of amorphous
aggregations (marine snow) in the Northern Adriatic Sea. III.
Zooplankton interactions with marine snow. Mar. Ecol. Prog. Ser., 87,
135–146.
Maar, M., Visser, A. W., Nielsen, T. G. et al. (2006) Turbulence and
feeding behaviour affect the vertical distributions of Oithona similis
and Microsetella norvegica. Mar. Ecol. Prog. Ser., 313, 157– 172.
Mullin, M. M. (1969) Production of zooplankton in the ocean: the
present status and problems. Oceanogr. Mar. Biol. Ann. Rev., 7,
293 –314.
Nielsen, T. G., Løkkegaard, B., Richardson, K. et al. (1993) Structure
of plankton communities in the Dogger Bank area (North Sea)
during a stratified situation. Mar. Ecol. Prog. Ser., 95, 115–131.
Nielsen, T. G. and Andersen, C. M. (2002) Plankton community structure and production along a freshwater-influenced Norwegian fjord
system. Mar. Biol., 141, 707 –724.
Dagg, M. (1993) Sinking particles as a possible source of nutrition for
the large calanoid copepod Neocalanus cristatus in the subarctic
Pacific Ocean. Deep-Sea Res. I, 40, 1431–1445.
Ohtsuka, S. and Kubo, N. (1991) Larvaceans and their houses as
important food for some pelagic copepods. Bull. Plankton Soc. Japan,
535 –551.
Daro, M. H. (1988) Migratory and grazing behavior of copepods
and vertical distribution of phytoplankton. Bull. Mar. Sci., 43,
710–729.
Ohtsuka, S., Kubo, N., Okada, M. et al. (1993) Attachment and
feeding of pelagic copepods on larvacean houses. J. Oceanogr., 49,
115 –120.
653
JOURNAL OF PLANKTON RESEARCH
j
29
VOLUME
Paffenhöfer, G.-A. (1993) On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). J. Plankton Res., 15, 37–55.
Plough, H. and Grossart, H.-P. (2000) Bacterial growth and grazing
on diatom aggregates: respiratory carbon turnover as a function of
aggregate size and sinking velocity. Limnol. Oceanogr., 45,
1467– 1475.
Richardson, K., Visser, A. W. and Bo Pedersen, F. (2000) Subsurface
phytoplankton blooms fuel pelagic production in the North Sea.
J. Plankton Res., 22, 1663–1671.
Sato, R., Tanaka, Y. and Ishimaru, T. (2001) House production by
Oikopleura dioica (Tunicata, Appendicularia) under laboratory conditions. J. Plankton Res., 23, 415 –423.
Shanks, A. L. and Edmondson, E. W. (1990) The vertical flux of
metazoans (holoplankton, meiofauna, and larval invertebrates) due
to their association with marine snow. Limnol. Oceanogr., 35, 455– 463.
j
NUMBER
7
j
PAGES
641 – 654
j
2007
Steinberg, D. K., Silver, M. W. and Pilskaln, C. H. (1997) Role of
mesopelagic zooplankton in the community metabolism of giant
larvacean house detritus in Monterey Bay, California, USA. Mar.
Ecol. Prog. Ser., 147, 167– 179.
Tiselius, P. and Kiørboe, T. (1998) Colonization of diatom aggregates
by the dinoflagellate Noctiluca scintillans. Limnol. Oceanogr., 43,
154 –159.
Tiselius, P., Petersen, J. K., Nielsen, T. G. et al. (2003) Functional
response of Oikopleura dioica to house clogging due to exposure to
algae of different sizes. Mar. Biol., 142, 253– 261.
Titelman, J. and Fiksen, O. (2004) Ontogenetic vertical distribution
patterns in small copepods: field observations and model predictions. Mar. Ecol. Prog. Ser., 284, 49–63.
Shanks, A. L. and del Carmen, K. A. (1997) Larval polychaetes are
strongly associated with marine snow. Mar. Ecol. Prog. Ser., 154, 211–221.
Uye, S., Aoto, I. and Onbé, T. (2002) Seasonal population dynamicös
and production of Microsetella norvegica, a widely distributed but littlestudied marine planktonic harpacticoid copepod. J. Plankton Res.,
24, 143– 153.
Shanks, A. L. and Walters, K. (1997) Holoplankton, meroplankton,
and meiofauna associated with marine snow. Mar. Ecol. Prog. Ser.,
156, 75– 86.
Vargas, C. A., Tönnesson, K., Sell, A. et al. (2002) Importance of
copepods versus appendicularians in vertical carbon fluxes in a
Swedish fjord. Mar. Ecol. Prog. Ser., 241, 125– 138.
Steinberg, D. K. (1995) Diet of copepods (Scopalatum vorax) associated
with mesopelagic detritus (giant larvacean houses) in Monterey Bay,
California. Mar. Biol., 122, 571–584.
Vidal, J. (1980) Physioecology of zooplankton. I. Effects of phytoplankton concentration, temperature, and body size on the
growth rate of Calanus pacificus and Pseudocalanus sp. Mar. Biol., 56,
111 –134.
Steinberg, D. K., Silver, M. W., Pilskaln, C. H. et al. (1994) Midwater
zooplankton communities on pelagic detritus (giant larvacean
houses) in Monterey Bay, California, USA. Limnol. Oceanogr., 39,
1606– 1620.
Webber, M. K. and Roff, J. C. (1995) Annual structure of the copepod
community and its associated pelagic environment off Discovery
Bay, Jamaica. Mar. Biol., 123, 467–479.
654