Journal of Experimental Marine Biology and Ecology 329 (2006) 174 – 186
www.elsevier.com/locate/jembe
Feeding and territorial behavior of Paralvinella sulfincola,
a polychaete worm at deep-sea hydrothermal vents of
the Northeast Pacific Ocean
Damien Grelon a,b, Marie Morineaux a,b, Gaston Desrosiers b, S. Kim Juniper a,c,*
a
b
GEOTOP Research Centre, Université du Québec à Montréal, P.O. Box 8888, Downtown Postal Station, Montréal (Québec), Canada H3C 3P8
Institut des Sciences de la mer de Rimouski (ISMER), Université du Québec à Rimouski, 310 des Ursulines, Rimouski (Québec), Canada G5L 3A1
c
Département des Sciences Biologiques, Université du Québec à Montréal, P.O. Box 8888, Downtown Postal Station, Montréal (Québec),
Canada H3C 3P8
Received 15 March 2005; received in revised form 17 August 2005; accepted 23 August 2005
Abstract
Behavioral adaptations to the severe nature and high faunal densities of hydrothermal vent habitats have received little attention
from researchers. In this study, video and digital still imagery were analyzed to document the feeding and general behavior of the
polychaete Paralvinella sulfincola at deep-sea vents on the Juan de Fuca ridge (North-East Pacific). This worm lives in mucous
tubes on the actively growing portions of sulphide mineral chimneys and is considered to be the pioneering macrofaunal species in
this habitat. We identified 6 recurrent behavior patterns, including antagonistic territoriality between neighboring conspecifics. The
latter likely explains the regular spatial distribution of P. sulfincola populations on the substratum they colonize, and the observed
confinement of feeding and exploration activities to a definable territory around the tube opening. Territory size, territorial overlap
and density were significantly related to body weight, further supporting the importance of size and aggressive encounters in the
maintenance of the worm’s feeding area. During feeding, P. sulfincola uses its buccal tentacles to gather particles from the
substratum using two different capture modes: seizing single macro-particles and aggregation of small particles.
D 2005 Elsevier B.V. All rights reserved.
Keywords: Feeding behavior; Hydrothermal vents; Juan de Fuca Ridge; Paralvinella sulfincola; Spatial distribution; Territorial behavior
1. Introduction
Deep-sea hydrothermal vents host dense, high biomass assemblages of benthic invertebrates nourished by
the chemolithoautotrophic production of organic matter
by bacteria that oxidize hydrogen sulphide and other
* Corresponding author. GEOTOP Research Centre, Université du
Québec à Montréal, P.O. Box 8888, Downtown Postal Station, Montréal (Québec), Canada H3C 3P8. Tel.: +1 514 987 3000x6603; fax:
+1 514 987 3635.
E-mail address: [email protected] (S.K. Juniper).
0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2005.08.017
reducing substances present in hydrothermal fluids
(Grassle, 1985; Tunnicliffe, 1991). While most vent
species are endemic to this habitat, all are related to
organisms found in other marine benthic habitats and
their ability to exploit the energy-rich deep-sea vents
appears to be related to a combination of physiological
and behavioral adaptations. Considerable research effort has been directed at understanding the physiology
of vent organisms, particularly in relation to invertebrate–microbial symbioses (Nelson and Fisher, 1995;
Van Dover, 2000) and mechanisms that permit vent
species to tolerate the hydrogen sulphide (Martineu et
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
al., 1997; Zal et al., 1998) and heavy metals that are
abundant in vent fluids (Cosson and Vivier, 1997;
Yurkov and Csotonyi, 2003). In contrast, behavioral
adaptations have received considerably less attention,
despite high macrofaunal densities (Sarrazin and Juniper, 1999) that suggest competition for space, and sharp
physico-chemical gradients that require motile organisms to respond to temperature and chemical signals.
The alvinellid worms, found at hydrothermal vents
in the Eastern Pacific, are pioneering species that colonize the most severe hydrothermal vent habitats where
they can constitute the major part of the biomass (Fustec et al., 1987; Desbruyères and Laubier, 1991; Sarrazin and Juniper, 1999). Worms of the genus Alvinella,
175
the Pompeii worms, live in tubes on black and white
smoker chimneys at vents on the East Pacific Rise, and
have been observed actively moving at temperatures in
excess of 50 8C. At hydrothermal vent fields in the
Northeast Pacific, a related species known as Paralvinella sulfincola Desbruyères and Laubier, the sulfide
worm, occupies a similar habitat on high temperature
sulphide mineral edifices (Tunnicliffe et al.). Populations of P. sulfincola frequently form monospecific
colonies on hydrothermal chimney surfaces, along a
front between tolerable physico-chemical conditions
and bare surfaces where temperatures are too high for
colonization (Juniper et al., 1992; Sarrazin et al., 1997).
Temperatures of 20–80 8C have been measured on
Fig. 1. (A–D) Spatial distribution of Paralvinella sulfincola populations in sulfide edifice habitats on the S&M edifice complex, Endeavour
Segment, Juan de Fuca Ridge. (A) Evenly distributed P. sulfincola population on bulbous chimney at 9 m from edifice base. (B) Dense P. sulfincola
population on sulfide flange near edifice base. (C) Transition from P. sulfincola population at growing edge of sulfide flange to mixed community of
vestimentifera, limpets and other polychaetes on older surfaces. Same flange as in (B). (D) Several populations (circled) of P. sulfincola on approx.
1.5 m high chimney in upper reaches of edifice.
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D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
surfaces colonized by P. sulfincola (Juniper et al., 1992)
and Lee (2003) has recently shown that P. sulfincola
can survive experimental exposure to temperatures up
to 50–56 8C. Adult sulphide worms are 20–70 mm long
and live in a mucous tube, occasionally open at both
ends, which they secrete and attach to the mineral
substratum (Tunnicliffe et al., 1993). Tubes are multilayered and are colonized by filamentous microorganisms, particularly on the outer surface (Juniper, 1994).
Both solitary and aggregated tubes can be found in the
same habitat. Aggregated tubes are joined longitudinally, often forming a star or fan pattern, and individual
worms in the aggregates each have their own tube
opening.
Adult sulfide worms first appear on newly formed
substrata during early stages of secondary mineralization when decreasing porosity of chimney walls reduces
outward diffusion of high temperature fluids, lowering
temperatures and toxin concentrations to tolerable
levels. Time-series imagery (Juniper et al., 1992)
showed that the sulfide worms responded behaviorally
to the growth of sulphide edifices, by migrating and
building new tubes in order to remain near the leading
edge of accreting mineral surfaces (Fig. 1). Where
chimney growth is rapid, worm colonization can advance at a rate of 1 cm or more per day (Juniper et al.,
1992), although other observations (Juniper, unpublished) suggest that more stable worm populations
and substrata are also common. The Juniper et al.
(1992) study and others (Tunnicliffe, 1988; Juniper,
1994; Morineaux et al., 2002) proposed that P. sulfincola derives its nutrition by deposit feeding or grazing
on microbial biofilms that form on the substratum
surface. The worm has a typical detrivorous buccal
morphology, including buccal tentacles.
The fact that P. sulfincola usually forms monospecific
colonies on the substratum has permitted the species to
be used as a model system to study the influence of vent
invertebrates on hydrothermal mineralization (Juniper et
al., 1992) and on microbial growth and diversity (Juniper, 1994; Pagé et al., 2004). In these studies, interpretation of the worm’s influence on other processes has not
been confounded by the presence of other macrofaunal
species. In the study reported here, we further exploit
these single species colonies to gain some first insights
into the role of behavior in controlling the exploitation of
substrata and food resources by non-symbiotic vent
organisms. Individual P. sulfincola are abundant and
easily observed against the bare rock surface that they
colonize, and the near-absence of other macrofaunal
species simplifies the interpretation of behavior. This
species does occasionally colonize more stable parts of
sulfide chimneys, as part of the so-called high-flow tubeworm assemblage (Sarrazin and Juniper, 1999). However, the behavior of the sulfide worms in this habitat
cannot be observed without severe disturbance (i.e. removing the overlying tubeworms), so observations were
confined to the much more common, single-species
colonies. We examined the feeding behavior of P. sulfincola in order to identify how and where food was
acquired, and used behavioral observations to define the
size of individual feeding areas and their degree of
overlap. Early in our observations, we discovered evidence for territoriality, and the study was expanded to
allow further investigation of this phenomenon.
2. Material and methods
2.1. Study sites
2.1.1. Axial Volcano
Seafloor imaging and sampling work were carried
out using the remotely operated submersible ROPOS.
All samples of P. sulfincola populations and most video
recordings for behavioral studies were obtained in the
ASHES vent field (1545 m. depth) on Axial Volcano
(Juan de Fuca Ridge, 45V95WN, 130VW), a hydrothermally active seamount that sits astride the Juan de Fuca
Ridge (Fig. 2). Worm populations were studied at three
hydrothermal edifices in the ASHES field: the Hell,
Phoenix-Hillock and Medusa edifices, ranging in height
from 1 m (Medusa) to 8 m (Hell), were visited between
1998 and 2003. All sites occur within a radius of 20 m.
Fig. 2. Location of the Juan de Fuca Ridge, in the northeast Pacific
Ocean.
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
Worms were sampled using the ROPOS suction sampling device fitted with 200 Am filters, or by collection
of portions of mineral chimney with one of the ROPOS
manipulator arms. Sampled worm populations were the
source of information for all quantitative behavioral
studies and population studies.
2.1.2. Endeavour segment
Additional video recordings and digital photos were
acquired during ROPOS dives on the Main Endeavour
hydrothermal vent field (2200 m depth, Lat. 47857VN,
Long. 129808 W), located on the Endeavour Segment
of the Juan de Fuca Ridge (Fig. 2). Imagery was
collected from populations on the Smoke and Mirrors
and Salut edifices in 2001–2003.
2.2. Behavioral observations
2.2.1. Seafloor video recordings and digital imaging
All imagery was acquired from cameras mounted on
ROPOS during dive programs between 1997 and 2003.
Most behavioral studies used video imagery from 1998
and 1999 ROPOS dives. Video records were obtained
using a Sony DXC-990, three-CCD colour camera
equipped with a 16 optical zoom. The field of view
was illuminated using 3 1000 W arc lamps plus several incandescent lamps, all mounted on the bow of the
submersible. Video signals from the ROPOS camera
were transmitted as RGB or Component video through
a fibre optic cable to the support vessel, where they
were recorded on Betacam or S-VHS tape. Dives in
2002 and 2003 were also recorded in digital video
format on MiniDV and DVCam tape. Because of the
small size of the study subjects, considerable care was
taken to optimize the quality of video recordings. Two
parallel lasers mounted 100 mm apart on the camera
body provided scale in video images. Image scaling for
each analyzed surface used a 2-step calibration of digitized video frames, designed to minimize error resulting from the flattening of substratum relief in 2-D
images, and from operator inaccuracies during onscreen measurements in images. For the first scaling
step, digitized video frames representing 3 different
viewing angles of the same surface were selected, and
scale was fixed in each frame from the laser points,
using the IP Lab SpectrumR software package (Grehan
and Juniper, 1996). Next, the distance between a pair of
objects visible in all three frames was measured 3 times,
using the SpectrumR measurement tool and each frame’s respective calibration. The mean (n = 9) distance
between the two objects was then used to scale the
scene, using SpectrumR, for all viewing angles. Scenes
177
where the coefficient of variation for the scaling measurements exceeded 5% were excluded from quantitative analyses.
Digital still photos were acquired with a deep-sea
version of the Sony Cyber-Shot DSC-F707 five megapixel digital camera, remotely controlled from the surface. Photos were used to illustrate distribution and
behavior patterns. For the latter, several 20-s interval
photo time-series were taken, in order to capture the
different behavior patterns. The digital still camera
used the submersible’s arc and incandescent lights for
illumination.
2.2.2. Image analysis
For behavioral studies, video imagery was analyzed
using an analog S-VHS video editing suite to control
tape playback, identify behavioral patterns and determine their duration, to document behavioral sequences
and to compile separate tapes of individual behavioral
patterns for detailed analysis. Some of the feeding
behavior studies, conducted in 2002 and 2003 used
digital video recordings, which were analyzed using a
similar approach on a computer-based digital editing
system (Apple’s Final Cut Pro).
Worm distribution, density and feeding area were
quantitatively determined from digitized video frames,
using the laser scaling technique outlined above. A
biometric tool was also developed for in situ determination of wet weight of individual worms from
mean length of branchiae measured on-screen in
digitized video frames. The latter determination used
a linear regression (r 2 = 0.933, n = 457, P b 0.001) of
body weight (wet) versus mean length of branchiae,
derived from sampled populations of P. sulfincola
from these same study locations (Grelon, 2001).
The branchiae were consistently visible in imagery
and frequently spread out over the substratum where
several could be measured for each individual. The
dark colour of the branchiae contrasted sharply with
the light-coloured substratum. The detection limit for
this method was a body weight of 101.6 mg body
weight (wet), which corresponds to a body length of
1.83 mm.
Digital still images, available later in our study, were
primarily used for high-resolution documentation of
behavioral sequences observed in video imagery, and
to study the colonization of P. sulfincola tubes by
smaller P. sulfincola and other organisms.
2.2.3. Spatial distribution and individual activity areas
The spatial distribution of individual worms in P.
sulfincola populations was studied in digitized video
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frames, using the described laser scaling method to
superimpose a cm-scale x–y grid on digital images,
and assign x–y coordinates to individual tube openings.
The regularity or non-regularity of worm (tube opening) distribution patterns were then determined objectively by Nearest Neighbor Analysis (Clark and Evans,
1954), using the Spatial Pattern Analysis software developed by Fernandez et al. (1993).
The substratum surface area utilized by individual
worms was determined from repeated viewings of the
10-min observation sequences. Points delimiting the
extremities of the zone explored by the worm, in relation to its tube opening, were marked on a scaled,
digitized video frame and a contour was drawn by
joining points. The area encompassed by the contour
was quantified using the area tool in IP Lab
SpectrumR. Activities areas were determined for all
visible worms at the Sanctuaire site during the first
and second visits, as well as for all worms seen during
the third visit to the Pork Chop site, plus 10 more
worms randomly selected from the other sites. In situ
wet weight estimates, using the method described
above, were derived from digitized images of these
same worm populations, in order to examine the relationship of individual worm size to activity area and
behavioral patterns.
2.2.4. Behavioral repertoire and time budget
Video recordings of P. sulfincola populations varied
in length from 10 to 30 min. A preliminary analysis
revealed 6 recurrent behavior patterns, all of which
could be observed within a 10-min time interval.
Extending the observation period to 15 min in several
test populations yielded no significant change in frequency of behavioral patterns (Grelon, 2001). A seventh behavior, migration, was seen only rarely (see
below). The frequency and duration of individual recurrent behavior patterns were therefore determined
from 10-min video playback observation sessions,
where worm activity was noted at 1-s intervals. A
total of 75 individual worms at different sites within
the ASHES vent field were separately observed, with a
minimum of 10 individuals per site.
2.2.5. General behavior patterns
Repeat patterns and order of occurrence of the 6
recurrent behaviors were analyzed using transition matrices (Lehner, 1979). Frequencies of preceding and
following behaviors were tabulated for each behavior
pattern and significant transitions were recognized by
simple approximation derived from Castellan’s (1965)
method of partitioning contingency tables. By this
method, any cell in the transition matrix with a transformed frequency greater than v 20.05 (1 1/r) (df = 1;
r = number of categories) was considered significant
beyond the 0.05 level. The transformed frequency
was determined as the observed frequency minus the
expected frequency, divided by the square root of the
expected frequency. The expected frequency for each
cell is equal to the product of the corresponding row
and column divided by the total number of behaviors
(Miron et al., 1992).
2.2.6. Feeding behavior
Feeding behavior patterns were analyzed using the
approach developed by Goerke (1976) for the polychaete Nereis virens. Later in the study, a special effort
was made to obtain close-up images of particle capture
by P. sulfincola, using its buccal tentacles. Most video
recordings used for behavioral observations were down
looking, resulting in the buccal apparatus being obscured by the branchial crown.
3. Results
3.1. Spatial distribution
3.1.1. Regularity of distribution
The overall mean density of P. sulfincola populations across all sites was 34.1 individuals/dm2
(S.D. = 9.8, n = 9). At the Sanctuaire and Pork Chop
sites, densities fluctuated over a 10-day period between
repeat visits (Sanctuaire—33.7, 47.6 and 31.7 ind./dm2;
Pork Chop—26.3 and 46.9 ind./dm2). Four of the six P.
sulfincola populations studied had significant regular
distributions of individuals on the substratum (Nearest
Neighbor Analyses), while for the other two, the analyses could not identify a statistically significant
( P b 0.05) distribution pattern (Table 1). Two of the
sites with regular distributions maintained their patterns
during repeat visits over a 12-day period in 1998. There
was no apparent relationship between worm density
and distribution patterns.
3.1.2. Activity area
The 20–70-mm-long worms explored a substratum
area ranging from 25 to 2500 mm2, with a mean of
488.7 mm2 (S.D. = 386.5). While there were no significant between-site differences in mean activity area,
individual areas varied by a factor of up to 100 within
a given site. Among the 70 individual activity areas
mapped, overlap of activity areas between neighboring
individuals averaged 48.5% (S.D. = 27.6), and ranged
from 1.9% to 100%.
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
179
Table 1
Distribution and density of Paralvinella sulfincola populations at different hydrothermal vent sites in the ASHES vent field of Axial Volcano, Juan
de Fuca Ridge
Site
Observed distribution
Area analyzed
Sanctuaire—first visit
Sanctuaire—second visit
Sanctuaire—third visit
White Land
Shut Down
Dog Nose
Medusa—first visit
Medusa—second visit
Pork Chop—first visit
Pork Chop—second visit
Regular (*)
Regular (**)
Regular (***)
Random (ns)
Regular (***)
Regular (**)
Random (ns)
Random (ns)
Regular (*)
Regular (**)
14 7
10 7
12 21
99
11 22
10 16
14 14
11 15
14 10
8 13
(98 cm2)
(70 cm2)
(252 cm2)
(81 cm2)
(242 cm2)
(160 cm2)
(196 cm2)
(165 cm2)
(140 cm2)
(104 cm2)
Worm density
(ind/dm2 F S.D.)
33.5 F 8
47.6 F 8
31.7 F 5
30.3 F 5
38.5 F 6
16.1 F 5
35.8 F 8
14.3 F 2
26.3 F 3
46.7 F 7
Repeat visits occurred between September 4 and 16, 1998. Distribution patterns determined by nearest neighbor analysis. Statistical significance of
analyses indicated in parentheses (***P b 0.001; **P b 0.01; *P b 0.05; ns = not significant ( P N 0.05)). Worm density was determined from counts
in complete or partial 7 7 cm quadrats.
3.2. Behavior patterns
3.2.1. General behavior patterns
A total of 7 behavior patterns were initially identified:
1. Tube exploration—a worm’s branchial crown can be
observed moving over a tube or the edges of a tube,
not necessarily its own tube, making a brushing
movement with its branchiae. During this movement, the posterior portion of the worm always
remains within its tube even when tube exploration
involves substantial lateral movement and extension
of body segments.
2. Substratum exploration—begins with the worm
partly leaving its tube, maintaining only its posterior
extremity within the tube. The branchial crown is
fanned out over the substratum and extended away
from the tube in a succession of touching or brushing movements across the mineral surface. Extension can progress to a point where the worm is
almost completely out of its tube.
3. Forecourt sweeping—involves a slight extension of
the apical portion of the worm out of its tube, and
back and forth movement along the substratum near
the tube entrance. The frequency of these movements was quite variable, from very slow to more
rapid, and body extension was usually less than the
length of the branchiae.
4. Inactivity – the worm is motionless. The branchial
crown remains at the tube entrance or slightly inside.
It can be seen agitating slightly its branchial apparatus while remaining in contact with the tube opening or the substratum but the worm’s body shows no
movement.
5. Contact with a conspecific—defined as one P. sulfincola touching or being touched by another individual of the same species. The contact can involve
touching of the branchiae or contact of one individual’s branchiae and the median body segments of
another. Although contact is more a consequence of
exploration behavior than a separate behavioral act,
contacts were frequent and influenced subsequent
behavior (see below).
6. In-tube—the worm is completely withdrawn inside
its tube and no portion of its body was visible, not
even the branchiae.
7. Migration—an individual completely leaves its tube
and moves freely over the substratum with its entire
body visible. This behavior was rare and only observed on 4 occasions, 3 of which followed physical
disturbance of the substratum by the submersible.
Migratory behavior was not included in the data
analysis.
3.2.2. Behavioral time budget
Data from the 10-min observation sessions revealed
that P. sulfincola allocated disproportionate amounts of
time to the 6 primary behavioral patterns (Fig. 3).
Approximately half (53%) of the worm’s time was
spent in dinactivityT with a further 34% involved in
activities possibly related to searching for food (exploring substratum and tube surfaces and forecourt sweeping). The worms spent 11% of their time inside their
tubes and a final 2% in contact with conspecifics. The
mean duration of each behavioral pattern, before beginning another, varied from 61.5 s for rest (inactivity) to 5
s for contacts. Inactivity was the most frequently repeated behavior over the 10-min observation periods,
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D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
Fig. 3. Paralvinella sulfincola—selected morphological features and behavior patterns. (A) Branchiae (b) and buccal tentacles (t). (B) Hook in the
seventh setiger. (C) Inactivity, branchial crown remains at the tube (tu) entrance. (D) Exploration of the tube surface. (E) Substratum exploration. (F)
Contact with a conspecific. (G) Deposit feeding with buccal tentacles.
with nearly 6 (mean 5.98) separate occurrences per
period, representing 40% of recorded behavioral acts.
Combined tube and substratum exploration events
accounted for a further 32%, while forecourt sweeping
was relatively infrequent with 0.98 occurrences per 10min interval. Contacts with conspecifics were frequent,
with a mean of 2.26 encounters per 10 min or 13% of
total behavioral acts.
3.3. Behavioral sequences
Cells of the transition matrix (Table 2) for which the
transformed frequency was superior to v 2a (where
a = 0.25 to 0.025, df = 1) were accepted to represent
significant sequences and were plotted graphically
(Fig. 4). For values of a = 0.05, two major behavioral
loops can be identified, one cycling between inactivity
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
181
Table 2
Summary of the sequence of behavioral patterns by Paralvinella sulfincola
1
1 before
1 after
2 before
2 after
3 before
3 after
4 before
4 after
5 before
5 after
6 before
6 after
2
3
3
–3.67
–3.67
(α =0.5)
0.69
(α =0.5)
0.61
(α =0.025)
6.29
(α =0.05)
3.89
–0.84(α =0.25)
2.61
–0.74
–0.99
(α =0.1)
2.85
–0.65
(α =0.025)
5.97
(α =0.1)
2.83
–1.37(α =0.05)
4.66
–2.36
–1.17
3
4
5
6
13
14
8
20 (12)
67 (4)
82 (1)
56 (5)
75 (2)
23 (11)
32 (10)
35 (8)
18 (14)
42 (6)
14
9
12
40 (7)
69 (3)
5
6
4
1
0
3
17 (15)
33 (9)
20 (13)
5
(α =0.25)
2.15
(α =0.5)
0.10
–0.76
–0.19
–0.62
–2.09
(α =0.0)
3.73
–0.78
(α =0.05)
4.13
(α =0.5)
0.37
–1.29
(α =0.05)
4.12
Data come from 10-min observations of 75 individual worms. The behaviors are: (1) tube exploration, (2) substratum exploration, (3) forecourt
sweeping, (4) inactivity, (5) contact with a conspecific, (6) in tube. In shaded portion of table (upper right), numbers indicate the total number of
observations for each behavioral transition. Numbers in parentheses indicate rank order for the 15 most frequent transitions. Unshaded portion of
table (lower left) shows transformed frequencies with positive values indicating favored transitions with a values for v 2 tests in parentheses.
Transformed frequency = (observed frequency expected frequency)/square root of expected frequency.
and tube exploration, and another where the worm
passes from inactivity to exploration of the substratum
followed by contact with a conspecific and ending with
a return to the tube and the resumption of inactivity
(Fig. 3, Table 2).
Fig. 4. Behavior succession patterns. Arrow width is proportional to
alpha values for v 2 tests on transition matrix in Table 2. Two major
(a V 0.05) behavioral loops are identifiable, one cycling between
inactivity and tube exploration, and another where the worm passes
from inactivity to exploration of the substratum followed by contact
with a conspecific and ending with a return to the tube and the
resumption of inactivity.
3.4. Detailed behavior analysis
Contact with conspecifics, and substratum and tube
exploration were singled out for in-depth observation,
as the former sometimes led to physical striking, whereas the two exploration behaviors were possibly related
to searching for and acquiring particulate food. The
original 10-min video sequences were reviewed in detail to determine the frequency of striking incidents and
particle capture, and additional close-up video imagery
was collected for detailed study of movements and
body parts involved in both striking and particulate
feeding.
3.4.1. Physical striking
Physical contact between neighboring conspecifics
occasionally resulted in a highly stereotypic behavior.
Following initial contact, one individual would contract
its branchiae, recoil its body while rotating its apical
portion and then rapidly strike in the direction of the
other worm. Subsequently, both individuals would return to their tubes and became inactive. During these
strikes, physical contact involved the sub-branchial
body segments of the instigator striking the branchiae
of its neighbor. In P. sulfincola, the seventh setigerous
segment has modified parapodial setae in the form of
posteriorly curving hooks (Fig. 3). Close-up video
sequences showed that when the worm rotates its apical
region, the modified setae protrude from the body. An
individual can thus lead with its setae as it strikes.
Frequently, the setae hooked the branchial filaments
of the other worm, sometimes pulling it across the
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substratum as the striker withdrew into its own tube.
Video analysis did not permit determination of whether
or not this action resulted in tissue damage, although
the struck individual quickly returned to its tube once
released. Usually only a single strike followed an initial
contact, although repeat strikes were also observed.
Only 3.3% of a daily average of 325 physical contacts
per worm led to striking incidents, which had a mean
duration of 7 F 3.5 s. However, even at this rate, an
individual worm would still be involved in nearly 10
(mean = 9.76) aggressive encounters per day with a
neighboring conspecific. Only 24 of the 75 study individuals were the initiators in these encounters.
3.4.2. Body size versus behavior
No correlations were observed between behavioral
activity patterns (time budgets, behavioral sequences)
and individual wet weights. In contrast, wet weight and
individual activity areas were positively correlated
(r 2 = 0.21, p b 0.0001), while wet weight was negatively
correlated (r 2 = 0.21; p = 0.004) with proportion of the
activity area shared with neighbors. Larger individuals
thus had a larger activity area, which they shared less
with their neighbors than did smaller individuals. There
was also a positive correlation between the size of the
activity area and both the frequency and the duration of
the combined exploration behaviors (substratum plus
tube exploration (for both r 2 = 0.12, p = 0.0029). Finally,
the mean wet weight of worms occupying a distinct
tube was significantly superior to the mean wet weight
of worms observed living in aggregated tubes (one-way
ANOVA, p = 0.0005).
3.5. Feeding behavior
3.5.1. Particle capture
Like other polychaete worms, P. sulfincola captures
and ingests food particles using its buccal tentacles,
which are deployed ventrally as the worm moves over
the substratum. Much of the time the buccal tentacles
were obscured from the camera by the branchiae, but
occasionally favorable camera angle and substratum
orientation permitted direct observation of the tentacles
working the substratum and tube surfaces. However,
because of the masking effect of the worm’s body, it
was not possible to determine the frequency with which
searching activities resulted particle capture. Worms
were observed seizing particles with their buccal tentacles on four occasions, on both the substratum and on
their tube or on the tube of a neighboring conspecific.
This was followed by a return to the tube entrance
(inactivity) with the seized particle. Two different
food particle capture methods were observed: capture
of single macroscopic particles (3 observations), plus
one collection of several microparticles to form an
aggregate on the buccal tentacles. One worm was observed reworking a captured particle in front of its tube.
4. Discussion
Field behavioral studies need to consider the influence of observational methodology and environmental
factors when planning and interpreting observations.
For deep-water organisms with well-developed photoreceptor organs, such as some hydrothermal vent shrimp
(Kuenzler et al., 1997), methodological and interpretation problems may arise from the use of artificial
illumination for behavioral studies. For such animals
not normally exposed to light, behavior could be altered by the technology used to observe them. Although dermal and cephalic photoreceptors occur in
some annelids, none has been observed in the alvinellid
polychaetes (D. Desbruyères, personal communication), so that for this study, light effects on behavior
were assumed to be negligible. With regard to environmental factors, since the worms are isolated from
diurnal cycles in the surface ocean, the time of day was
not taken into account when planning or conducting
observations. Because the worms are exposed to severe
hydrothermal conditions, fluctuations in vent output
may have had some impact on behavior. However,
the frequency and duration of behavioral activities
showed a generally robust pattern across sites and
between repeat observations at the same site. We conclude, therefore, that the first-order behavior patterns
reported here were not significantly affected by environmental variability, with the exception perhaps of
occasional migration provoked by sustained and substantial changes in hydrothermal flow.
Earlier studies of the activity of benthic invertebrates
focused on feeding behavior, deposit or suspensionfeeding rates and particle selection in relation to food
availability and environmental conditions (e.g. Cammen, 1989; Taghon, 1982; Taghon et al., 1980). More
recent research has included inter- and intra-specific
interactions (Miron et al., 1991; Rosenberg et al.,
1997), responses to environmental change (Lambert et
al., 1992, Taghon and Greene, 1992; Ouellette et al.,
2004), diurnal activity patterns (Lambert et al., 1992)
and territoriality (Miron et al., 1992). While the behavioral repertoires are known only for a few benthic
invertebrates (Evan, 1971; Miron et al., 1992; Grelon,
2001), some generalization is possible, if only to permit
hypothesis development. For sedentary benthic inverte-
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
brates, extension or movement of all or part of the
animal into the space surrounding its resting position,
can usually be attributed to food prospecting, or to
territorial behavior (Miron et al., 1992; Levin, 1981;
Duchêne and Rosenberg, 2001). Other identified activities include regular or intermittent oxygenation (Tunnicliffe et al., 1990; Osovitz and Julian, 2002) and
thermoregulation (Chevaldonné et al., 1991), occasional tube or burrow maintenance and reproductive behavior (Herpin, 1925; Chevaldonné and Jollivet, 1993).
The two recurrent behavioral patterns in P. sulfincola in which there was no visible locomotory activity
(inactivity and in-tube) are probably the most straightforward to interpret. Since the worms spent more than
half (53%) of their time stopped and partially withdrawn into their tubes with their branchiæ deployed
(inactivity), we assume that this represents the normal
resting position where they oxygenate their gills while
minimizing physical effort and risk. During this behavior, P. sulfincola could also rework or manipulate food
particles captured with its buccal tentacles. Considerably less time (11%) was devoted to in-tube behavior.
Since the branchiæ are retracted as the worm withdraws
into its tube, thus limiting gas exchange, it is improbable that this behavior is related to normal rest. It more
likely involves essential tube maintenance or withdrawal in reaction to environmental fluctuations. Withdrawing into the tube also permits the polychaete to
occasionally reverse itself and exit at the opposite end
of the open tube, providing access to a greater feeding
area. The frequency of this latter behavior or openended tubes is uncertain. We observed reverse exiting
on fewer than 10 occasions, and sampled tubes were
usually too damaged to determine whether they had one
or two openings.
We interpret the exploration and sweeping behaviors
to be primarily related to the search for food and the
capture of particles. While the movement of the branchial crown may aid gas exchange, close-up video and
photos showed that the buccal tentacles were extended
and in direct contact with the substratum during these
behavioral sequences, and that particles were being
seized and retained, from both the substratum and
tube surfaces. In addition to probing for food, the
sweeping movements may also serve to dislodge or
separate lighter particles from the mineral substratum.
Other deposit feeders can efficiently resuspend finer
particles, which have higher nutritional value, by
sweeping the substratum with buccal palps (Self and
Jumars, 1978). These observations support earlier proposals that P. sulfincola feeds by grazing on microbial
biofilms on the mineral substratum (Tunnicliffe, 1988;
183
Juniper, 1994; Morineaux et al., 2002), and also identify the worm’s tube as a second food source. The tubes
of P. sulfincola are heavily colonized by a mixed
microbial community that shows some taxonomic differences with the microflora colonizing the mineral
substratum (Pagé et al., 2004). Morineaux et al.
(2002) found that P. sulfincola tubes were richer in
organic matter than sampled mineral substrata, although
some of the tube organic matter is produced by the
worm itself, in the form of mucous secretions. In order
for the tubes to be a sustainable food source, removal of
organic material by the worm would have to be balanced by production of new material by the tube microbial community.
Our observations of the reworking of macroparticles and collection of microparticles by P. sulfincola
could be interpreted as evidence for selective feeding.
However, the broad range in stable carbon isotope
values (up to 6.9x) within individual populations of
P. sulfincola observed by Levesque et al. (2003) indicates considerable individual variation in diet, and
suggests an opportunistic feeding strategy. This does
not preclude some particle selection, but the severe
and dynamic nature of the P. sulfincola habitat would
tend to favor a more generalist and adaptable feeding
strategy.
In isolation, the frequent physical contact, and possibly even the stereotypic recoil and striking observed
between neighboring P. sulfincola might be interpreted
to be related to mating activity, as described by Herpin
(1925) in some Terebellomorph polychaetes to which
the family Alvinellidae belongs. Indeed, possible reproductive behavior has been proposed to explain occasional brief entry into neighboring tubes by Alvinella
spp., which colonizes hydrothermal chimneys at East
Pacific Rise hydrothermal vents (Chevaldonné and Jollivet, 1993). However, this study provides several lines
of evidence to support the hypothesis that contact and
strikes in P. sulfincola are related to territoriality, in
particular to the maintenance of feeding territory. To
begin, the various elements of the stereotypic recoil and
striking behavior appear more typical of aggression
than mating or exchange of gametes. We suggest that
the frequency of these encounters (10 per day per
individual), the use of the hook, the multiple strikes,
the dragging of the neighbor from its tube and the
withdrawal of both parties after the strikes all point to
antagonistic rather than reproductive behavior. All
physical contacts between neighboring worms appear
important to the maintenance of territory. Our analysis
identified a recurrent behavioral loop where contacts
between conspecifics, even when they did not result in
184
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
strikes, resulted in the abrupt cessation of exploration
activity and a return to the inactivity position at the tube
opening.
The statistically regular distribution of P. sulfincola
populations over a range of densities, on both uniform
and highly heterogeneous substrata, suggests a behavioral mechanism for controlling use of space (Davies,
1978; Levin, 1981). Further, observations confirmed
that exploration and feeding activity of individual
worms were limited to a definable area around the
tube opening, except for occasional migrations that
resulted in the construction of a new tube and the
establishment of a new activity area. In addition, we
found a positive correlation between an individual’s
body size and its activity area, and a significant negative correlation between activity area overlap and body
size. This would suggest that food resource requirements are influencing distribution patterns of P. sulfincola populations, and we argue that these patterns are
maintained through aggressive behavior; larger individuals maintain exclusive control over larger areas of
substratum (and food resources). Alternatively, nonaggressive competitive effects between neighbors
adjusting to food resource depletion could produce
the observed spacing pattern. However, we did not
observe any correlation of density with the regularity
of worm distribution patterns nor with activity area size
or overlap (Grelon, 2001). Body size seems to be the
primary determinant of access to space (and food
resources) on the substratum. We therefore propose
that aggressive behavior more than resource abundance,
is controlling the distribution of P. sulfincola populations. This contrasts with the findings of Miron et al.
(1992), who concluded that aggression in N. virens was
limited to competition for burrow space and did not
control spatial distribution.
Fighting and territorial defense have been documented in burrow-dwelling and errant nereid polychaetes
(Reish and Alosie, 1968; Evan, 1971; Miron et al.,
1992). Territoriality and intra- and inter-specific competition have been little studied in the hydrothermal
vent environment. While reducing substances in hydrothermal fluids can fuel high levels of biomass production by autotrophic microorganisms (McCollom and
Shock, 1997), vent communities are restricted to a
narrow zone around vent openings where the mixing
of hydrothermal fluids with oxygenated seawater permits chemosynthesis by symbiotic and free living
microbes. Potential competitors from the surrounding
deep sea are usually excluded from this mixing zone by
the severe physico-chemical conditions. Within the
fluid discharge zone, substratum space provides access
to the local food supply, creating potential for competition among vent consumer species, including those
with symbionts. The dense packing of vent invertebrates such as bivalves, tubeworms, shrimp and gastropods within the fluid discharge zone underlines the
importance of space in this habitat. For sedentary deposit feeding species such as P. sulfincola, it is reasonable to anticipate that, while at one level population size
will be controlled by local productivity conditions, the
maintenance of individual feeding areas could contribute to stabilizing populations.
In all studied populations, small individual P. sulfincola occurred mostly on the tubes of adults. Smaller
adults often formed aggregates of attached tubes, while
those worms occupying solitary tubes were significantly larger than those living in attached tubes. Together
with the migration behavior observed here and elsewhere (Juniper et al., 1992; Grelon, 2001), these observations suggest a predictable ontogenic and behavioral
control of substratum utilization by the sulfide worm.
We present this in the form of a conceptual model,
where there is a progression from larval settlement
through to the occupation of solitary tubes by larger
adult individuals. After settlement on the substratum or
on adult tubes, small worms first appear in imagery
attached to the tubes of larger individuals. We can then
identify an intermediate stage where several worms
occupy attached tubes. The latter are frequently further
back from the mineralization front than the solitary
tubes, suggesting that migration and the construction
of tubes on newly available substrata may be more
frequent in larger individuals. Our observation data do
not permit direct comparison of behavior patterns between aggregated and solitary worms, although the
size-related comparisons would suggest that, compared
to solitary worms, smaller adults occupying aggregated
tubes exploit smaller activity areas that overlap more
with those of neighboring conspecifics. The entire colonization process merits further systematic study since
tube building by P. sulfincola can influence the mineralogical and ecological evolution of sulfide chimneys.
The tubes have been proposed to accelerate, or at least
focus, the deposition of marcasite (FeS2) on the surface
of sulfide chimneys and so reduce chimney wall porosity (Paradis et al., 1988 Juniper et al., 1992). This, in
turn, has been suggested to permit colonization by other
species (Sarrazin et al., 1997). The mediation of ecological succession by P. sulfincola tube building is not
limited to effects on metazoans. Preliminary evidence
also indicates that sulfide worm tubes harbor a microbial flora that is distinct from that colonizing the adjacent substratum (Pagé et al., 2004). Since the tubes also
D. Grelon et al. / J. Exp. Mar. Biol. Ecol. 329 (2006) 174–186
appear to serve as a food source for P. sulfincola, the
facilitation of microbial growth on tubes (i.e. microbial
gardening) also merits further investigation.
Morineaux et al. (2002) estimated energetic requirements for individual sulfide worms in relation to potential productivity of the feeding area. Although approximate, these calculations indicate that microbial
primary production within feeding area would need to
be quite high, within the upper range of production
rates by photosynthetic microorganisms in other benthic habitats, in order to sustain the worm populations.
This also supports the use of the tube microflora as an
additional food source and brings into question the
long-term sustainability of grazing by P. sulfincola
populations. Migration may, in fact, be an important
behavioral response to diminishing food availability at
time scales beyond those observed here. As mineralization progresses on the surfaces colonized by the
sulfide worms, the porosity of the sulfide substratum
decreases (Juniper et al., 1992; Sarrazin et al., 2002).
This will reduce the hydrothermal fluid supply to microbial populations on the chimney surface, to the point
where it may reduce chemosynthetic productivity available to the worms. Alternatively, migration may be
driven by population growth (Rosenberg et al., 1997).
The observational time scale employed in this study did
not permit detection of any relationship between migration frequency and worm density. In fact, testing of
most aspects of the space utilization model proposed
here for P. sulfincola will require continuous, timeseries studies of individual populations over a period
of many months.
Acknowledgements
We thank the ROPOS team, the crews of the NOAA
ship Ronald H. Brown and J.P. Tully for their support at
sea, and Glenn Juniper for the photo of P. sulfincola
used in Fig. 3A. Luc-Alain Giraldeau and three anonymous reviewers provided helpful comments on an
earlier version of this manuscript. This research was
supported by the Natural Sciences and Engineering
Research Council of Canada (NSERC) grants to SKJ
and GD. [RH]
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