Introduction
Deep-sea hydrothermal vents occur along mid-ocean ridges and back-arc
spreading centres, which are characterised by strong volcanic and tectonic
activity. The resulting hydrothermal fluid fosters dense communities of
highly specialised fauna that colonise the steep physical and chemical
gradients created by the mixing of hot vent fluids with cold seawater. These
communities are distributed according to species' physiological tolerance
(Childress and Fisher, 1992; Luther et al.,
2001), resource availability
(De
Busserolles et al., 2009; Levesque et al., 2003) and biotic interactions
(Lenihan
et al., 2008; Micheli et al., 2002; Mullineaux et al., 2000, 2003). Although
the fauna are highly dissimilar between oceanic basins
(Bachraty et al., 2009; Moalic et al.,
2011), hydrothermal communities throughout the world share some ecological
similarities including a food web based on chemosynthesis
(Childress and Fisher, 1992), low species diversity compared
with adjacent deep-sea and coastal benthic communities
(Van Dover and Trask, 2000; Tunnicliffe, 1991),
high levels of endemism (Ramirez-Llodra et al.,
2007), and elevated biomass associated with the presence of large
invertebrate species.
The high spatial heterogeneity of environmental conditions in vent
ecosystems is amplified by stochastic and periodic temporal variation in
hydrothermal activity, influencing the composition
(Sarrazin et al., 1999), structure
(Marcus
et al., 2009; Sarrazin et al., 1997; Tsurumi and Tunnicliffe, 2001) and
dynamics
(Lelièvre
et al., 2017; Nedoncelle et al., 2013, 2015; Sarrazin et al., 2014) of
faunal communities. In addition, the complexity of vent habitats is
increased by engineer species, whose presence strongly contributes to the
modification of the physical (temperature, hydrodynamics processes) and
chemical (hydrogen sulfide, methane, oxygen, metals and other reduced
chemicals) properties of the environment either by creating
three-dimensional biogenic structures (autogenic species) or through their
biological activity (allogeneic species) (Jones et al.,
1994, 1997). Habitat provisioning and modification by engineer species
increases the number of potential ecological niches and, consequently,
influences species distribution and contributes to an increase in local
diversity
(Dreyer
et al., 2005; Govenar and Fisher, 2007; Urcuyo et al., 2003). Engineer
species promote local diversity through various ecological mechanisms
(Bergquist et al., 2003), providing a secondary
substratum for colonisation, a refuge from predation and unfavourable
abiotic conditions, and important food sources that enhance the development
of macro- and meiofaunal communities
(Dreyer
et al., 2005; Galkin and Goroslavskaya, 2010; Gollner et al., 2006; Govenar
et al., 2005, 2002; Govenar and Fisher, 2007; Turnipseed et al., 2003;
Zekely et al., 2006).
Hydrothermal vent food webs are mainly based on local microbial
chemosynthesis (Childress and Fisher, 1992), performed by
free-living or/and symbiotic chemoautotrophic microorganisms that utilise
the chemical energy released by the oxidation of reduced chemicals species
(H2, H2S, CH4) present in the hydrothermal fluids
(Childress and Fisher, 1992). Several electron donors (e.g. H2, H2S, CH4, NH4+) and electron acceptors
(e.g. O2, NO3-, SO42-) can be used by these
microorganisms as energy sources, converting inorganic carbon (e.g. CO2) into simple carbohydrates (Fisher et al., 2007).
Chemosynthetic primary production is exported to the upper trophic levels
through direct ingestion (primary consumers) or through the presence of
intra- or extracellular symbiosis. Upper trophic levels (secondary
consumers) are represented by local predators and scavengers feeding on
primary consumers and by abyssal species attracted by the profusion of food.
Stable isotopes analysis is an important and efficient tool in studying
trophic ecology and offers many advantages over traditional methods
(behavioural observations, stomach content analyses), providing
the time-integrated overview of an animal's diet over a long timescale.
Nevertheless, the physiology of marine invertebrates is poorly documented,
resulting in a lack of precision on the turnover rate of an organism's tissue
and therefore, the rate at which a consumer integrates the isotopic signal,
leading to an uncertainty about trophic-step fractionation (isotopic
enrichment between preys and predators). Moreover, although trophic
inferences using stable isotopes require the characterisation of basal
sources, this remains difficult in the hydrothermal environment due to technological sampling constraints. Despite this, the emergence of isotopic
methods has opened new perspectives in the understanding of food web
functioning and the organisation of species diversity within these
ecosystems around the globe
(Bergquist
et al., 2007; De Busserolles et al., 2009; Van Dover, 2002; Erickson et al.,
2009; Gaudron et al., 2012; Levesque et al., 2006; Levin et al., 2009;
Limén et al., 2007; Portail et al., 2016; Soto, 2009; Sweetman et al.,
2013). The carbon isotope composition (δ13C) is an indicator of
the food assimilated and remains relatively constant during trophic
transfers (±1 ‰). The kinetics of enzymes
involved in the biosynthetic pathways of autotrophic organisms influence the
carbon isotope ratio (13C / 12C), allowing the discrimination
between the sources fuelling the community
(Conway et al., 1994; Van Dover and
Fry, 1989). Nitrogen isotope composition (δ15N) provides
information on trophic levels and becomes enriched in heavy isotopes at an
average rate of ±3.4 ‰
at each trophic level
(Michener and Lajtha, 2008). At the community scale, δ13C and δ15N signatures of all species in the ecosystem
are used to retrace carbon and nitrogen fluxes along the trophic chain and,
therefore, to reconstitute the food web (Levin and Michener,
2002). Despite the relatively low diversity of vent communities, ample
evidence suggests that hydrothermal food web structure is complex
(Bergquist
et al., 2007; Portail et al., 2016), including many trophic guilds
(Bergquist
et al., 2007; De Busserolles et al., 2009) and multiple sources of primary
production (Van Dover and Fry, 1994). The
carbon signature (δ13C) of primary producers differs according
to their carbon fixation pathways that differentially fractionate inorganic
carbon sources. Despite the fact that the nitrogen signature (δ15N) does not discriminate between primary producers, the variability of δ15N signatures can be associated with their origins and also with local
biogeochemical processes
(Bourbonnais
et al., 2012; Portail et al., 2016). Moreover, due to its degradation in the
water column, photosynthesis-derived organic matter is characterised by high
δ15N values in comparison with local vent microbial producers,
which are associated with low or negative values characteristic of local
inorganic nitrogen sources (Conway et al., 1994).
(a) Location of the Juan de Fuca Ridge system and the seven
segments (yellow diamonds). (b) High-resolution bathymetric map of the
Endeavour Segment, with the locations of the five main active vent fields
(white triangles). (c) Location map of the Main Endeavour vent field
indicating the positions of hydrothermal vent edifices (black diamonds).
(d) Bathymetric map of the Grotto active hydrothermal edifice
(47∘56.958′ N, 129∘5.899′ W). The 10 m high sulfide structure
is located in the Main Endeavour vent field.
Active hydrothermal vents on the Juan de Fuca Ridge (north-east Pacific) are
colonised by populations of the siboglinid polychaete Ridgeia piscesae forming dense faunal
assemblages in areas of high to low fluid flux activity
(Southward et al., 1995). Diverse heterotrophic faunal
species inhabit these tubeworm bushes, with a dominance of polychaete and
gastropod species
(Bergquist
et al., 2007; Govenar et al., 2002; Marcus et al., 2009; Tsurumi and
Tunnicliffe, 2001, 2003). To date, few studies have described the
communities associated with the R. piscesae tubeworm assemblages of the Main Endeavour
vent field, either in terms of diversity
(Bergquist
et al., 2007; Sarrazin et al., 1997) or trophic ecology
(Bergquist et al., 2007). Six
distinct faunal assemblages exhibiting patchy distributions have been
identified on the Smoke and Mirrors hydrothermal edifice, and appear to
represent different successional stages
(Sarrazin et al., 1997). Since 2011, a
camera installed on the Ocean Networks Canada cabled observatory has been recording
high-resolution imagery of a R. piscesae tubeworm assemblage and its associated fauna
on the active Grotto hydrothermal edifice (Main Endeavour, Juan de Fuca
Ridge). The processing of this data provided new insights into the influence
of astronomic and atmospheric forcing on vent faunal dynamics
(Cuvelier et al., 2014;
Lelièvre et al., 2017), but thorough knowledge of the faunal communities
observed by the camera is still needed to understand and interpret the
temporal patterns and their underlying mechanisms. However, although video
imagery is useful for investigating the spatial distribution of communities
(Cuvelier et al., 2011;
Sarrazin et al., 1997), species behaviour
(Grelon et al., 2006; Matabos et al.,
2015) and temporal dynamics of a subset of species
(Cuvelier et al., 2014;
Lelièvre et al., 2017), direct sampling is an essential and
complementary approach for determining overall faunal composition, abundance
and species diversity and assess functioning
(Cuvelier et al., 2012). In this context, the
objectives of the present study were (i) to identify the composition and
structure of three faunal assemblages associated with R. piscesae tubeworm bushes on
the Grotto hydrothermal edifice, specifically with respect to density,
biomass and species diversity, (ii) to characterise the trophic structure of
these biological communities, and (iii) to assess how diversity and trophic
relationships vary over different successional stages.
Hydrothermal samples collected on the Grotto edifice (Main
Endeavour Field, Juan de Fuca Ridge) during Ocean Networks Canada
oceanographic cruises Wiring the Abyss 2015 and 2016.
Results
Species–effort curves, tubeworm structural complexity and
diversity
The rarefaction curves (excluding Ridgeia piscesae; Fig. 3) showed that, overall, the
collected samples (S1 to S6) gave a fairly good representation of the
species diversity on the Grotto hydrothermal edifice. In 2015, sample S2 (24
species) and S3 (31 species) rarefaction curves seemed to reach a plateau.
S1 consisted of a total of 28 macrofaunal species. The samples from the year 2016
exhibited lower species richness and did not reach an asymptote. Samples S4
and S5 both had a macrofaunal species richness of 19 species, while only 14
species were found in sample S6 (Fig. 3).
Tubeworm surface areas and volumes of the samples were used as proxies for
habitat complexity provided by the engineer species R. piscesae
(Table 2). Samples S1 and S3 were characterised by a similar degree of
structural complexity, with a tubeworm surface of 4.27 and
4.26 m2, respectively (Table 2). Sample S2 displayed a sampling
area of less than half of that of S1 and S3 reaching a total tubeworm
surface area of 1.63 m2. Samples from 2016 were substantially
smaller than those from 2015. Tubeworm surface areas varied between 0.1 and
0.57 m2. To summarise, the tube
surface areas of the different samples were as follow:
S1 > S3 > S2 > S5 > S6 > S4 (Table 2). Sample volumes
were also strongly correlated (Radj2=0.82;
p value = 0.008) to the tubeworm surface area for these Grotto
samples and thus can be used as an easily measurable proxy to estimate
habitat complexity.
Alpha diversity measures showed that S4 displayed the lowest diversity (D=2.605; 1-λ′=0.550), followed by S6 (D=3.998; 1-λ′=0.633) and S5 (D=4.348; 1-λ′=0.697). The highest
diversity values observed were S1 (D=5.377; 1-λ′=0.728),
slightly less than S2 (D=5.398; 1-λ′=0.749) and S3
(Shannon D=6.053; 1-λ′=0.778). The S2 and S3 samples showed
a more even distribution (J′) of individuals among species than the other
samples. In contrast, S4 had the lowest evenness (J′=0.325) (Table 2).
Species richness was significantly correlated with R. piscesae tube length
(Radj2=0.62; p value = 0.039).
Percentage abundance × 100 (% Ab.), faunal density (D. ind m-2), volume (V. indm-3) and relative
biomass × 100 (% Biom.) of the different macrofaunal taxa
(> 250 µm) identified in the six sampling units (S1 to S6) on
the Grotto edifice. The taxa were identified to the lowest possible
taxonomical level.
Species
S1 – assemblage V low flow
S2 – assemblage V low flow
S3 – assemblage V low flow
S4 – assemblage IV
S5 – assemblage V low flow
S6 – assemblage III
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
% Ab.
D. (indm-2)
V. (indm-3)
% Biom.
Annelida
Polychaeta
Maldanidae
Nicomache venticola
0.1
8
1604.5
0.2
0.1
14.1
7033.6
0.1
0.2
35.5
6363.3
1.1
0
0
0
0
0
0
0
0
0
0
0
0
Dorvilleidae
Ophryotrocha globopalpata
0.1
4.2
849.5
< 0.1
0.1
9.8
4893
< 0.1
1.3
202
36 241.1
< 0.1
< 0.1
1.8
934.6
< 0.1
< 0.1
10
1851.9
< 0.1
0
0
0
0
Orbiniidae
Berkeleyia sp. nov.
0
0
0
0
0
0
0
0
< 0.1
6.3
1137.8
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Hesionidae
Hesiospina sp. nov.
0.1
9.8
1982.1
< 0.1
0.1
10.4
5198.8
< 0.1
0.1
14.3
2570.6
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Phyllodocidae
Protomystides verenae
< 0.1
0.5
94.4
< 0.1
< 0.1
0.6
305.8
< 0.1
< 0.1
0.2
42.1
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Polynoidae
Branchinotogluma tunnicliffeae
< 0.1
0.7
141.6
< 0.1
0.1
9.2
4587.2
< 0.1
< 0.1
2.6
463.6
< 0.1
0.2
47.4
25 233.7
0.2
< 0.1
20
3703.7
< 0.1
0.3
16.4
400
< 0.1
Branchinotogluma sp.
0
0
0
0
0
0
0
0
0
0
0
0
< 0.1
1.8
934.6
< 0.1
0
0
0
0
0
0
0
0
Lepidonotopodium piscesae
0
0
0
0
< 0.1
1.2
611.6
< 0.1
< 0.1
3.8
674.3
< 0.1
0.2
43.9
23 364.5
0.9
0.1
50.1
9259.3
0.2
0.2
10.9
266.7
0.1
Levensteiniella kincaidi
0.1
8.2
1651.7
0.1
0.1
10.4
5198.8
< 0.1
< 0.1
4
716.4
< 0.1
< 0.1
3.5
1869.2
< 0.1
< 0.1
20
3703.7
< 0.1
0
0
0
0
Sigalionidae
Pholoe courtneyae
< 0.1
0.2
47.2
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Syllidae
Sphaerosyllis ridgensis
3.6
257.6
51 911.3
< 0.1
1
170.2
85 015.3
< 0.1
1.7
262.6
47 113.4
< 0.1
0
0
0
0
0.1
90.1
16 666.7
< 0.1
0.1
5.5
133.3
< 0.1
Alvinellidae
Paralvinella dela
0
0
0
0
0
0
0
0
< 0.1
0.7
126.4
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Paralvinella palmiformis
0
0
0
0
0.1
10.4
5198.8
< 0.1
0.1
10.3
1854.2
0.1
3.3
726.4
386 915.9
6.8
0.2
110.2
20 370.4
0.8
0.7
43.6
1066.7
1.4
Paralvinella pandorae
< 0.1
0.7
141.6
< 0.1
< 0.1
2.5
1223.2
< 0.1
0.1
17.4
3118.4
< 0.1
0.1
17.6
9345.8
< 0.1
0.1
70.1
12 963
< 0.1
5.4
354.3
8666.7
< 0.1
Paralvinella sulfincola
0
0
0
0
0
0
0
0
< 0.1
6.6
1179.9
0.1
0.6
122.8
65 420.6
0.5
0.1
70.1
12 963
< 0.1
5.4
354.3
8666.7
< 0.1
Ampharetidae
Amphisamytha carldarei
26.8
1932.1
389 334.6
0.5
24.5
3367.5
1 681 651.4
0.5
34.8
5378.8
964 938.9
1.8
0.4
80.7
42 990.7
< 0.1
< 0.1
10
1851.9
< 0.1
0.2
10.9
266.7
0.1
Ctenodrilidae
Raricirrus sp.
< 0.1
0.2
47.2
< 0.1
0
0
0
0
< 0.1
1.9
337.1
< 0.1
0
0
0
0
5.1
3004.6
555 555.6
0.2
7.4
479.6
11 733.3
0.1
Spionidae
Prionospio sp.
< 0.1
2.1
424.7
< 0.1
0
0
0
0
< 0.1
0.9
168.6
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Mollusca
Aplacophora
Simrothiellidae
Helicoradomenia juani
3.7
263.7
53 138.3
< 0.1
3.4
461.1
230 275.2
< 0.1
5.6
861.9
154 614.4
0.14
0.1
17.6
9345.8
< 0.1
1.3
791.2
146 296.3
< 0.1
2
130.8
3200
< 0.1
Gastropoda
Buccinidae
Buccinum thermophilum
0.1
9.8
1982.1
3.2
0.1
18.4
9174.3
1.6
< 0.1
2.4
421.4
0.4
0
0
0
0
0.1
50.1
9259.3
5.8
0
0
0
0
Provannidae
Provanna variabilis
1.9
137
27 607.4
2.2
1.6
224.8
112 232.4
1.3
4.5
694.8
124 652.3
6.8
0.3
61.4
32 710.3
0.3
8.6
5117.8
946 296.3
10
1.8
114.5
2800
0.4
Peltospiridae
Depressigyra globulus
10.8
779.9
157 149.6
1.1
14.5
1986
991 743.1
1.1
20.1
3105.4
557 100.7
2.9
51.4
11 294.7
6 015 887.9
13
44
26 179.8
4 840 740.7
21
23.2
1515.1
37 066.7
1.5
Clypeosectidae
Clypeosectus curvus
0.5
34.7
6984.4
0.1
0.2
20.2
10091.7
< 0.1
< 0.1
6.8
1222.1
< 0.1
0
0
0
0
0.1
50.1
9259.3
< 0.1
0
0
0
0
Lepetodrilidae
Lepetodrilus fucensis
42.7
3083.1
621 283.6
12.5
39.5
5429.4
2 711 315
10.1
22.8
3519.5
631 394.9
11.5
43
9457.6
5 037 383.2
19.4
30.1
17 907.2
3 311 111.1
18.1
55
3586.1
87 733.3
18.2
Arthropoda
Arachnida
Halacaridae
Copidognathus papillatus
4.9
349.6
70 457.8
< 0.1
1.5
211.9
105 810.4
< 0.1
4.9
754.7
135 398.2
< 0.1
< 0.1
8.8
4672.9
< 0.1
< 0.1
60.1
11 111.1
< 0.1
0
0
0
0
Amphipoda
Alicellidae
Paralicella cf. vaporalis
< 0.1
1.6
330.3
< 0.1
< 0.1
6.1
3058.1
< 0.1
< 0.1
3.1
547.8
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Calliopiidae
Oradarea cf. walkeri
< 0.1
4.7
943.8
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Leptamphopus sp.
0
0
0
0
0
0
0
0
0
0
0
0
< 0.1
3.5
1869.2
< 0.1
0
0
0
0
0
0
0
0
Crustacea
Philomedidae
Euphilomedes climax
0.7
52
10 476.6
< 0.1
10.9
1502.2
750 152.9
0.1
0.2
23.3
4171.9
< 0.1
0.3
70.2
37 383.2
< 0.1
9.1
5378.2
994 444.4
< 0.1
3.3
218
5333.3
< 0.1
Cytherudidae
Xylocythere sp. nov.
2.9
206.8
41 670.6
< 0.1
1.4
188
93 883.8
< 0.1
2.7
413
74 083.4
< 0.1
< 0.1
7
3738.3
< 0.1
0.3
170.3
31 481.5
< 0.1
0.1
5.5
133.3
< 0.1
Pycnogonida
Ammotheidae
Sericosura verenae
0.6
42.6
8589.0
< 0.1
0.6
84.5
42 201.8
0.5
0.7
113.5
20 354
0.8
0.1
24.6
13 084.1
0.2
0.6
360.6
66 666.7
1.2
0.4
27.3
666.7
0.2
Sericosura venticola
0.2
15.2
3067.5
< 0.1
0.1
8
3975.5
0.5
< 0.1
1.9
337.1
0.8
< 0.1
1.8
934.6
< 0.1
0
0
0
0
0
0
0
0
Sericosura cf. dissita
0.1
5.6
1132.6
< 0.1
< 0.1
1.2
611.6
0.5
< 0.1
0.7
126.4
0.8
0
0
0
0
0
0
0
0
0
0
0
0
Nemertea
Unidentified
< 0.1
1.2
236.0
< 0.1
0
0
0
0
< 0.1
2.8
505.7
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Echinodermata
Ophiuroidea
< 0.1
0.2
47.2
< 0.1
0
0
0
0
< 0.1
0.5
84.3
< 0.1
0
0
0
0
0
0
0
0
0
0
0
0
Composition and structure of Grotto vent communities
The species list and abundances for each sample collected within the Grotto
hydrothermal edifice are provided in Table 3. A total of 148 005 individuals
representing 35 macrofaunal species (excluding Ridgeia piscesae) were identified in the six
tubeworm bushes (S1 to S6) sampled on the Grotto edifice. Overall,
gastropods (5 species) and polychaetes (18 species), respectively, accounted
for 69.5 ± 18.8 % and 16.3 ± 11.8 % of the total
macrofaunal abundance. The numerically most abundant species were the
gastropods Lepetodrilus fucensis and Depressigyra globulus as well as the polychaete Amphisamytha carldarei. The highest macrofaunal
densities were observed in samples S5 (59 450 indm-2), S4
(23 784 indm-2), S3 (15 452 indm-2) and S2
(13 748 indm-2), whereas S1 and S6 had the lowest densities, with
7212 and 6518 indm-2, respectively. A high percentage
(30 %) of the species was only found in one or two samples.
More specifically, S1 was dominated by gastropod species such as L. fucensis, D. globulus and
Provanna variabilis (Table 3). High densities contrasted with low biomass were observed for the
ampharetid polychaete A. carldarei and the syllid polychaete Sphaerosyllis ridgensis. S2 was also dominated by
L. fucensis, D. globulus and A. carldarei,
with, however, a high proportion of ostracods Euphilomedes climax (Table 3). S3 was
largely dominated by A. carldarei and, to a lesser extent, was almost equally dominated
by L. fucensis and D. globulus. Polychaetes were also dominant, with the presence of S. ridgensis, the
dorvilleid Ophryotrocha globopalpata and the maldanid Nicomache venticola. There were high densities
of P. variabilis, the
solenogaster Helicoradomenia juani, the halacarid
Copidognathus papillatus, the ostracod Xylocythere sp. nov. and the pycnogonid Sericosura verenae (Table 3).
S4 was dominated by L. fucensis and D. globulus and, to a lesser extent, by the alvinellid
polychaete Paralvinella palmiformis (Table 3). S5 was also dominated by
L. fucensis and D. globulus, followed by E. climax and P. variabilis
(Table 3). Finally, S6 was also dominated L. fucensis and D. globulus and, to a lesser extent, by
A. carldarei and the alvinellid polychaete Paralvinella pandorae (Table 3).
Stable isotope bi-plots showing vent consumers' isotope signatures
(mean δ13C versus δ15N values ± standard deviation)
for the six vent assemblages sampled on the Grotto hydrothermal edifice. Each
vent species is designated by a number: 1 – Ridgeia piscesae; 2 –
Provanna variabilis; 3 – Depressigyra globulus; 4 –
Lepetodrilus fucensis; 5 – Buccinum thermophilum; 6 –
Clypeosectus curvus; 7 – Amphisamytha carldarei; 8 –
Branchinotogluma tunnicliffeae; 9 – Lepidonotopodium piscesae; 10 – Levensteiniella kincaidi; 11 – Nicomache venticola; 12 – Paralvinella sulfincola; 13 –
Paralvinella palmiformis; 14 – Paralvinella pandorae; 15
– Paralvinella dela; 16 – Hesiospina sp. nov.; 17 –
Sphaerosyllis ridgensis; 18 – Ophryotrocha globopalpata;
19 – Berkeleyia sp. nov.; 20 – Protomystides verenae; 21
– Sericosura sp.; 22 – Euphilomedes climax; 23 –
Xylocythere sp. nov.; 24 – Copepoda; 25 – Copidognathus papillatus; 26 – Paralicella cf. vaporalis; 27 –
Helicoradomenia juani. Known trophic guilds are distinguished by a
colour code: pink – symbiont; green – bacterivores; blue –
scavengers/detritivores; red – predators. For more information on the
interpretation of guilds, please consult the web version of this paper.
δ13C and δ15N isotopic composition
δ13C values of the vent fauna ranged from -33.4 to
-11.8 ‰ among the different samples (Fig. 4). In more
details, δ13C values ranged from -33.4 to
-13.5 ‰ for S1, from -33.4 to
-15.4 ‰ for S2 and from -32.4 to
-14.7 ‰ for S3. Samples from S4, S5 and S6 displayed
slightly narrower δ13C ranges, varying from -30.3 to
-12.5 ‰, from -31.3 to
-14.8 ‰ and from -32.3 to
-11.8 ‰, respectively; most species were enriched in
13C relative to the S1, S2 and S3 samples (Fig. 4). Overall, the
gastropod Provanna variabilis (species no. 2) was the most depleted in 13C, with values
around -32.2 ‰ (±1.2 ‰).
In contrast, Ridgeia piscesae siboglinids (species no. 1) showed the highest δ13C values, with constant values around -14.7 ‰
(±1.0 ‰). The range of δ15N values
in faunal assemblages varied between -8.5 and 9.4 ‰
(Fig. 4). Especially, S1 values ranged from 0.3 to 8.4 ‰,
S2 from 0.4 to 9.2 ‰, S3 from -2.7 to
8.3 ‰, S4 from -1.3 to 8.7 ‰, S5
from -1.1 to 6.4 ‰ and S6 from -8.5 to
9.4 ‰ (Fig. 4). Generally, 15 species showed a δ15N > 5 ‰ in S1, S2 and S3 assemblages
but only 4 species were over 5 ‰ in δ15N in
S4, S5 and S6. In contrast to their δ13C values, P. variabilis and R. piscesae
displayed similar and relatively stable δ15N values among
samples with 0.3 ‰ (±0.8 ‰)
and 1.5 ‰ (±1.1 ‰),
respectively.
Stable isotope bi-plots showing vent consumers' isotope
signatures weighted by biomass per square metre of tubeworms (filled circles)
for the six vent assemblages (S1 to S6) sampled on the Grotto hydrothermal
edifice. Considered as a habitat, the biomass of Ridgeia piscesae
(denoted by a triangle symbol) is not shown. Each vent species is designated
by a number: 1 – Ridgeia piscesae; 2 – Provanna variabilis; 3 – Depressigyra globulus; 4 – Lepetodrilus fucensis; 5 – Buccinum thermophilum; 6 – Clypeosectus curvus; 7 – Amphisamytha carldarei; 8 – Branchinotogluma tunnicliffeae; 9 – Lepidonotopodium piscesae; 10 – Levensteiniella kincaidi; 11 – Nicomache venticola; 12 – Paralvinella sulfincola; 13 – Paralvinella palmiformis;
14 – Paralvinella pandorae; 15 – Paralvinella dela; 16 – Hesiospina sp. nov.;
17 – Sphaerosyllis ridgensis; 18 – Ophryotrocha globopalpata;
19 – Berkeleyia sp. nov.; 20 – Protomystides verenae;
21 – Sericosura sp.; 22 – Euphilomedes climax; 23 – Xylocythere sp. nov.;
24 – Copepoda; 25 – Copidognathus papillatus; 26 – Paralicella cf. vaporalis; 27 – Helicoradomenia juani.
For legibility, the biomass of P. pandorae in collection S6 is not shown.
Biomass distribution in Grotto vent food webs
The projection of the species isotopic ratios weighted by biomass is useful
for estimating the relative contributions of the different trophic pathways
within the vent assemblages (Fig. 5). In our study, there were similar
patterns of biomass distribution in the six sampled assemblages. In all six
samples, the ecosystem engineering polychaete Ridgeia piscesae (species no. 1) represented
the highest proportion of biomass (69.3 ± 16 %). However, as it was
considered to be a structuring species of the ecosystem, it was not included
in the following biomass distribution analysis. With a total proportion of
biomass ranging from 78.9 to 95.8 % (89.6 ± 6.8 %) across
samples, gastropods seemed to play an important role in the trophic food web
of communities associated with the siboglinid tubeworms. The gastropod
biomass was dominated by Lepetodrilus fucensis (species no. 4), which accounted for 31.5 to
82.8 % (55.8 ± 18.3 %) of the total biomass. In addition to L. fucensis,
the gastropods Depressigyra globulus (species no. 3),
Provanna variabilis (species no. 2) and Buccinum thermophilum (species no. 5) showed
relatively high proportions of biomass within the different samples, ranging
from 5.6 to 36.6 % (16.5 ± 13.8 %), 0.6 to 26.3 %
(10.9 ± 9.8 %) and 0 to 16.1 % (6.4 ± 6.8 %),
respectively (Fig. 5). However, in some samples, other species also
significantly contributed to the total biomass. For example, in S3, the
polychaete Amphisamytha carldarei (species no. 7) contributed substantially (7.2 %) to the total
biomass. Similarly, in S4, the polychaete Paralvinella palmiformis (species no. 13) contributed to
16.4 % of the total biomass.
Discussion
Communities and diversity
Hydrothermal ecosystems of the north-east Pacific are dominated by dense
populations of the tubeworm Ridgeia piscesae. In this study, a total of 36 macrofaunal species
(including R. piscesae) were found in the six tubeworm bushes sampled on the Grotto
edifice, which is consistent with previous knowledge of the community in the region
(Bergquist et al., 2007). In
this study, macrofaunal species richness was slightly lower than that
observed at the Easter Island hydrothermal site on the Main Endeavour Field,
where a total of 39 species has been identified in a single R. piscesae bush
(Bergquist et al., 2007).
Tsurumi and Tunnicliffe (2003) reported the presence of 39 macrofaunal
species in 25 collections from the Axial Segment (JdFR), but lower values
have been reported on other segments, with 24 species in seven collections from
the Cleft Segment (JdFR) and 19 species in two collections from the CoAxial
Segment (JdFR). These levels of diversity are lower than that found in
Riftia pachyptila bushes on the East Pacific Rise, where species richness in eight collections
reached 46 species (Govenar et al., 2005).
Macrofaunal diversity was also lower than those obtained in ecosystem
engineering mussel beds from Lucky Strike on the Mid-Atlantic Ridge, with 41
taxa identified
(Sarrazin
et al., 2015), or from the northern and southern East Pacific Rise, with
richnesses of 61 and 57 species, respectively (Van Dover, 2003).
Variation between sites and regions may be related to discrepancies in
sampling effort and methodologies. Alternatively, faunal dissimilarities
between biogeographic regions may be closely related to the geological
context, species colonisation history, connectivity to neighbouring basins,
presence of geographic barriers (transform faults, hydrodynamic processes,
depths, etc.), stability of hydrothermal activity, age of the vent system
and distances between sites (Van Dover et
al., 2002).
Tubeworm bushes sampled on the Grotto edifice were characterised by the
dominance of a few species such as Lepetodrilus fucensis, Depressigyra globulus and Amphisamytha carldarei. Numerical dominance by a few
species is a pattern that has also been reported from other hydrothermal
sites of the world oceans: the Mid-Atlantic Ridge
(Cuvelier
et al., 2011; Sarrazin et al., 2015), the East Pacific Rise
(Govenar et al., 2005), JdFR
(Sarrazin
and Juniper, 1999; Tsurumi and Tunnicliffe, 2001) and the southern East
Pacific Rise (Matabos et al.,
2011). Polychaetes were the most diverse taxa, representing half of the
macrofaunal species richness with 18 species. Similar results have been
reported within R. piscesae bushes on Easter Island, with the identification of 23
polychaete species (Bergquist
et al., 2007). Although the dominant species were similar among samples,
variation between samples mainly involved the relative abundance of the few
dominant species and the identity of the “rare” species. These variations
may result from differences in sampling strategies between years. The areas
sampled in 2016 were smaller than in 2015, and a problem with the sampling
boxes may have led to the loss of some individuals, even though not visible
from videos recorded by the submersible. Variation in species richness and
diversity among samples may also depend on the presence of environmental
gradients, created by the mixing between ambient seawater and hydrothermal
effluents (Sarrazin et al., 1999). Unfortunately,
no environmental data were recorded with our samples. However, physical and
chemical conditions are known to change along the ecological succession
gradient on the MEF from newly opened habitat characterised by high
temperature and sulfide concentrations, colonised by the sulfide worm
Paralvinella sulfincola, to mature communities in low diffuse venting areas characterised by low
temperatures and sulfide concentrations and colonised by long skinny R. piscesae
tubeworms (Sarrazin et al., 1997).
Tubeworm samples S1 and S3 were visually recognised as type V low-flow
assemblages (Sarrazin et al., 1997), an
advanced stage in the ecological succession characterised by longer tubes
(18.5 ± 3.3 cm) and thus a higher level of structural complexity.
Both samples showed the highest species richness, diversity and most complex
food webs, suggesting a strong influence of engineer species and the
importance of biogenic structure in the diversification and persistence of
the local resident fauna. By increasing the number of micro-niches available
for vent species, the 3-D structure of R. piscesae bushes helps to increase the
environmental heterogeneity and thereby promotes species richness and
diversity at assemblage scales
(Jones et al., 1997; Tsurumi and
Tunnicliffe, 2003). As mentioned by several authors
(Bergquist et
al., 2003; Govenar et al., 2002; Tsurumi and Tunnicliffe, 2003), various
ecological mechanisms may explain the influence of R. piscesae tubeworms on local
diversity: new habitats generated by tubeworm bushes provide (i) a substratum
for attachment and colonisation, (ii) interstitial spaces among intertwined
tubes, increasing habitat gradients and therefore the number of ecological
niches, (iii) a refuge to avoid predators and to reduce the physiological
stress related to abiotic conditions, and (iv) a control on the transport of
hydrothermal vent flow and nutritional resource availability. Samples S2 and
S5, also identified as type V low-flow assemblages
(Sarrazin et al., 1997), presented
shorter tube lengths than S1 and S3, which might explain the lower species
richness in these two samples. High densities of A. carldarei in R. piscesae tubeworm bushes (up to
93.4 %) may be related to this ampharetid's tolerance to environmental
conditions and, therefore, to their ability to take advantage of a wide
range of ecological niches (McHugh and
Tunnicliffe, 1994). Similar to L. fucensis, A. carldarei is characterised by early maturity and
high fecundity, contributing to the success of this species in vent habitats
(McHugh and Tunnicliffe, 1994). The dominance
of gastropods L. fucensis and D. globulus as well as the relatively high abundance of the
Paralvinella polychaete species in samples S4 and S6 suggest that they belong to lower
succession levels, corresponding to transitory states between types III and
IV assemblages described by Sarrazin et al. (1997). The latter two samples
were characterised by low species richness and diversities. We hypothesise
that the numerical dominance of gastropods negatively affected species
diversity by monopolising space and nutritional resources and by potentially
grazing new recruits, therefore reducing the settlement of other vent
species. As suggested by Sarrazin et al. (2002), the development of tubeworm
bushes along the successional dynamics leads to the diversification of
ecological and trophic niches, which may increase the complexity of the food
web.
Trophic structure of tubeworm assemblages
The Ridgeia piscesae tubeworm assemblages of the Grotto hydrothermal edifice harbour a
relatively diverse heterotrophic fauna. The isotopic analyses conducted on
the most dominant vent macrofaunal species within the bushes revealed a high
degree of resemblance in trophic structure among the six faunal samples. In
this study, the position of species in the food webs (trophic structure) was
consistent with the ones reported in Bergquist et al. (2007), with, however,
less variability in carbon and nitrogen stable isotopes.
Hydrothermal food webs are generally based on two main energetic pathways:
the transfer of energy from symbionts to host invertebrates and the
consumption of free-living microbial production
(Bergquist et al., 2007). In
the present study, the contrasting isotope compositions of the gastropods
Provanna variabilis, Lepetodrilus fucensis and the polychaete R. piscesae suggest a wide range of isotopically distinct,
symbiotic and/or free-living microbial production available to primary
consumers. The high δ13C values of R. piscesae were associated with
chemosynthetic endosymbiosis linked to thiotrophic symbionts
(Hügler and Sievert, 2011). Despite R. piscesae contributing to 86 %
of the total biomass, a low number of species displayed similar δ13C values, suggesting that specialist species deriving the majority
of their food sources from siboglinid tubeworms are rare. Similar
observations, where engineer species contribute to the community more as a habitat than as a food source, have been reported in R. piscesae tubeworm bushes from
the Easter Island vent site
(Bergquist et al., 2007) and in
Bathymodiolus azoricus mussel bed assemblages on the Tour Eiffel hydrothermal edifice (Lucky
Strike, Mid-Atlantic Ridge) (De
Busserolles et al., 2009). The low degree of exploitation of this large
biomass and potential food resource suggests that rather than playing a
trophic role, R. piscesae would primarily play a structuring role in vent ecosystems.
Nevertheless, the δ13C and δ15N values of
polynoids Branchinotogluma tunnicliffeae and Lepidonotopodium piscesae were consistent with a predatory diet including R. piscesae tubeworms.
Moreover, the predation of tubeworms by polynoids is often observed, as shown on a video sequence from the ecological observatory module TEMPO-mini,
deployed on the Grotto hydrothermal edifice (ONC observatory; Video S1 in the Supplement). The
13C-depleted stable isotope compositions of P. variabilis suggest a possible
symbiosis with chemoautotrophic bacteria or reliance on feeding on a very
specific free-living microbial community that depends on a 13C-depleted
carbon source (Bergquist et
al., 2007). To date, no study has reported the presence of chemoautotrophic
symbionts in P. variabilis, but symbioses have been described for other species from the
Provannidae family (Windoffer and Giere, 1997). With an
intermediate δ13C composition between R. piscesae and P. variabilis, L. fucensis gastropods seem
to represent a major energetic pathway in these vent communities. Food webs
obtained in this study revealed that most vent species display a δ13C similar to L. fucensis, but with slightly higher δ15N values.
Through its high densities, large biomasses and its position at the base of
the food webs, we suggest that L. fucensis could play an important role in structuring
vent communities. The wide-ranging feeding strategies of this limpet may
exert a high pressure on the availability of nutritional resources for
others vent species. Likewise, the range of feeding strategies open up more
opportunities for L. fucensis, allowing this limpet to take advantage of resources that
other species cannot. The four Paralvinella species observed in our samples, which are
described as suspension and/or deposit feeders
(Desbruyères and Laubier, 1986; Tunnicliffe
et al., 1993), displayed low or negative δ15N values. These
lowest δ15N values may be related to the nutrition of a
microbial pool based on local nitrogen sources. In fact, the ammonium
produced during the microbial degradation of organic matter appears to be
usually 15N-depleted (Lee and Childress, 1996). Amongst
these Paralvinella species, Paralvinella sulfincola,
Paralvinella palmiformis and Paralvinella dela shared the same isotopic niche while P. pandorae displays a
distinct isotopic composition.
Like in many vent food webs
(Van Dover
and Fry, 1994; Levesque et al., 2005; Limén et al., 2007), Grotto
primary consumers were dominated by grazers and deposit feeders (Table 1).
The high diversity, densities and biomass of bacterivores emphasise the
importance of free-living bacteria in the establishment and maintenance of
the structure of the vent food web
(Bergquist et al., 2007). The
bacterivore guild was mainly represented by the gastropods P. variabilis, Depressigyra globulus and L. fucensis and the
polychaetes P. sulfincola, P. palmiformis, P. pandorae
and P. dela. Like Paralvinella grasslei and Paralvinella bactericola at vent sites of the Guaymas Basin
(Portail et al., 2016), the alvinellid
species found at Grotto had comparable δ13C values but
different δ15N signatures. Paralvinella pandorae showed a depleted δ15N
signature relative to other alvinellid species. A previous study of isotope
variability among three sympatric alvinellid species, P. palmiformis, P. sulfincola and P. pandorae on the JdFR
reported that their differences in δ15N isotope composition
could be closely related to the presence of food-source partitioning and/or
to spatial segregation (Levesque et al.,
2003). The comparatively small size of P. pandorae compared with other alvinellid
species (Desbruyères and Laubier, 1986;
Tunnicliffe et al., 1993) may be linked to the presence of interspecific
competition for food resources and/or a diet based on an isotopically
distinct microbial source. The wide range of δ13C signatures in
bacterivores, coupled with the high interspecific variability in the
isotopic space, suggest a large, diversified microbial pool in the
hydrothermal ecosystem and high variability in isotope ratios in dominant
microbial taxa. Detritivore/scavenger species were observed at an
intermediate trophic level, between the bacterivore and predator feeding
guilds. This guild was represented by a low number of species including the
gastropod Buccinum thermophilum, the ampharetid Amphisamytha carldarei and the orbiniid Berkeleyia sp. nov. The predator feeding guild
was represented by the highest δ15N values. High predator
diversity was found in our vent assemblages and was associated with a wide
range of δ13C values, covering the isotopic spectrum of lower
trophic-level consumers (i.e. bacterivores as well as
scavengers/detritivores). This guild of predators appears to be dominated by
polychaetes, which tend to show the highest δ15N values. The
syllid Sphaerosyllis ridgensis, the polynoid Levensteiniella kincaidi and the hesionid Hesiospina sp. nov.
displayed the highest δ15N values, suggesting that they play the role of predators in the
benthic food web. Similarly, the solenogaster Helicoradomenia juani consistently displayed higher
δ15N values than other molluscs, indicating a predator trophic
position. The presence of Zoarcidae eelpouts Pachycara gymninium and Oregoniidae spider crabs
Macroregonia macrochira on the Grotto edifice, not sampled but observed in the video recorded by
the TEMPO-mini ecological module, could also play the role of predator
within the ecosystem. Except for the polynoid L. kincaidi, whose isotopic variability
seemed to reveal a nutrition based on highly diversified food resources,
stable isotope analyses conducted on predators revealed narrow ranges of
δ13C and δ15N values at the species scale,
suggesting the dominance of specialist feeding strategies, as was the case
for bacterivores. An accurate assessment of the isotopic composition of food
sources and a description of the meiofaunal communities would be necessary
to further increase our understanding of the functioning of these
chemosynthetic communities and their trophic structures.
Ecological niche partitioning
Vent species on the Grotto hydrothermal edifice exhibit high isotopic
heterogeneity that reflects the complexity of vent ecological food webs. The
distribution of species in the bi-dimensional isotopic space depends on
their diets, environmental conditions and biotic interactions, which
together define the concept of species ecological niche
(Newsome et al., 2007) or the realised species
trophic niche (Bearhop et al., 2004). Here, the
fact that most of the isotopic space was occupied by isotopically distinct
species shows that the available food resources are partitioned within the
community. Although the δ15N variability among primary
consumers did hinder our inference of trophic levels based on nitrogen
isotopes, these communities are unlikely to host more than three trophic
levels, given the overall δ15N ranges. Moreover, although
predators were quite diverse, they only represented a minor part of the
biomass, suggesting that Grotto vent communities are mostly driven by
bottom–up processes. Food webs of chemosynthetic ecosystems – such as
hydrothermal vents and cold seeps – do not appear to be structured along
predator–prey relationships but rather through weak trophic relationships
among co-occurring species
(Levesque et
al., 2006; Portail et al., 2016). Habitat and/or trophic partitioning are
important structuring processes at the community scale
(Levesque
et al., 2003; Levin et al., 2013; Portail et al., 2016). Our results
corroborate those from Axial Volcano in the JdFR
(Levesque et al., 2006) and the Guaymas
basin (Portail et al., 2016), where
habitat heterogeneity induces spatial partitioning of trophic niches,
leading to a spatial segregation of species and species coexistence
(Levesque et al., 2006). Although the
observed isotope variability (standard deviations) in Grotto vent species
suggests the occurrence of both trophic specialists and generalists within
the assemblages, the majority of vent species exhibited low standard
deviations, suggesting a predominantly specialist feeding behaviour. As
already shown in previous studies of vent sites with alvinellids
(Levesque et al., 2003) and sulfidic
sediments at methane seeps with dorvilleid polychaetes
(Levin et al., 2013) in the
north-east Pacific, food partitioning may occur between different species of
the same or related taxonomic family, allowing species coexistence through
the occupation of distinct trophic niches. Our study confirmed this pattern for
alvinellid polychaetes of the genus Paralvinella
(Levesque et al., 2006). Hydrothermal
vent gastropods were numerically dominant in all Ridgeia piscesae bushes collected on the
Grotto edifice, and their isotope compositions were fairly diverse.
Gastropods exhibit great diversity in feeding strategies, and as a result
they are found in a wide variety of niches where they exploit many food
sources
(Bates et
al., 2005; Bates, 2007). The isotope composition of Provanna variabilis indicated low δ13C and δ15N values. Lepetodrilus fucensis gastropods had higher δ13C and δ15N values than P. variabilis but a similar range of δ13C as Clypeosectus curvus and Depressigyra globulus. However, these latter two species occupy an upper
position in the trophic structure of their communities. The great ecological
success of L. fucensis in vent habitats may be attributed to a combination of several
characteristics. First, this species is characterised by a broad trophic
plasticity that includes (i) grazing on siboglinid tubeworms and hard
substrata (Fretter, 1988), (ii) active suspension feeding
(Bates, 2007), and (iii) harbouring filamentous
bacterial epibionts in its gills, which – via endocytosis – may contribute
to the animal's nutritional requirements
(Bates, 2007; Fox et al., 2002).
In addition, the early maturity, high fecundity and continuous gamete
production of L. fucensis may help to maintain the large populations on the edifice
(Kelly and Metaxas, 2007).
Stacking behaviour near fluid emissions also suggests that L. fucensis is an important
competitor for space and food in the community
(Tsurumi and Tunnicliffe, 2003). L. elevatus, the
ecological equivalent of L. fucensis on the East Pacific Rise, is prey for the vent
zoarcid fish Thermarces cerberus; the reduced limpet population promotes the successful
settlement and growth of sessile benthic invertebrates such as tubeworms
(Micheli
et al., 2002; Sancho et al., 2005). The potential absence of an equivalent
predator for L. fucensis and the biological characteristics detailed above may explain
its ecological success on the north-east Pacific vent sites. In contrast,
the nutrition of D. globulus is based on the grazing of organic matter only
(Warén and Bouchet, 1989). However, its small size allows it
to exploit interstitial spaces that are not available to larger fauna
(Bates et al., 2005). Finally, P. variabilis was
relatively less abundant than the other two species but appeared to exploit
a different thermal niche than L. fucensis and D. globulus
(Bates et al., 2005). On the other
hand, the isotope composition of Buccinum thermophilum clearly differentiates that species from
the other gastropods with higher δ13C signatures. Differences
in the diets of co-occurring species may contribute to the high abundance
and diversity of vent gastropods through niche partitioning
(Govenar et al., 2015).
Habitat specialisation among co-occurring vent species may drive differences
in their diets (Govenar et al., 2015), facilitating
species coexistence in heterogeneous habitats such as hydrothermal
ecosystems. We hypothesised that vent food webs display a small-scale
spatial structure that is linked to the 3-D architecture of the biogenic
structures generated by engineer species. This would promote high
interspecific trophic segregation. The spatial segregation of trophic niches
by environmental gradients limits the occurrence of biotic interactions such
as predation and competition for resources between species sharing a common
spatial niche (Levesque et al., 2006).
Vent food webs may therefore be structured through the interplay between the
availability and diversity of food sources and the abiotic and biotic
conditions structuring species distribution.