AÇOREANA, Suplemento 6, Setembro 2009: 201-210
THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL, AZORES, AND A
COMPARISON WITH OTHER AZOREAN INVERTEBRATE HABITATS
Roger N. Bamber & Roni Robbins
The Natural History Museum, Cromwell Road, London SW7 5BD, U.K. e-mail: [email protected]
ABSTRACT
During the Third International Workshop of Malacology and Marine Biology in the
Azores in July 2006, sampling of the littoral and sublittoral soft-sediment benthos around
Vila Franca do Campo, São Miguel, was undertaken in order to characterize the benthic
infaunal communities, and to compare the faunal density and diversity with the communities associated with algae.
The sedimentary infauna was particularly sparse, with the average number of species
and individuals per sample being 4.4 and 25 respectively. Although density and diversity
were greatest between 20 and 40 m depth, there was no community trend with depth
down to 250 m. The dominant taxa were actively mobile species. By contrast, the fauna
of algal habitats was far denser and more species rich: these samples had an average of 17
species and 360 individuals per sample.
These results indicate an unstructured, impoverished sedimentary infauna, dominated by errant taxa which can tolerate unstable sediments, and not well-characterized as a
community. The impoverishment of sedimentary benthos of this part of the Azores is
attributed to sediment instability.
SUMÁRIO
Durante o 3º Workshop Internacional de Malacologia e Biologia Marinha nos Açores
em Julho de 2006, foram feitas amostragens do bentos do sedimento móvel do litoral e
sublitoral perto de Vila Franca do Campo, São Miguel, com vista a caracterizar as
comunidades bentónicas da infauna e comparar a densidade e diversidade da infauna com
as comunidades associadas às algas.
A infauna sedimentar era particularmente esparsa, sendo o número médio de espécies
e indivíduos por amostragem 4,4 e 25, respectivamente. Embora a densidade e a
diversidade fossem as mais elevadas entre os 20 e os 40 m de profundidade, não se notou
tendência na comunidade com a profundidade até aos 250 m. Os taxa dominantes eram
espécies activamente móveis. Em contraste, a fauna dos habitats algais era de longe mais
densa e mais rica em espécies: ali se registou a média de 17 espécies e 360 indivíduos por
amostra.
Estes resultados indicam uma infauna sedimentar não estruturada, empobrecida,
dominada por taxa errantes que podem tolerar sedimentos instáveis, e não bem
caracterizada coo comunidade. O empobrecimento do bentos sedimentar desta parte dos
Açores atribui-se à instabilidade do sedimento.
INTRODUCTION
he Azores are a group of islands
somewhat isolated in the north-east
Atlantic, lying adjacent to the MidAtlantic Ridge some 1300 km west of
Portugal and 1730 km southeast of
T
Newfoundland. The main surface water
currents reaching the archipelago bring
waters from two directions: the Azores
Drift, a diffuse southerly arm of the Gulf
Stream breaking off from the North
Atlantic Drift supplies water from the
Americas, while the somewhat less-sig-
202
A Ç O R E A N A
nificant western eddies of the Canary
Current bring waters from Spain and
North Africa; below these, the midwater
current brings warm, hyperhaline water
from the Mediterranean outflow (Gofas,
1990; Morton et al., 1998; Morton &
Britton, 2000). This hydrography clearly
has implications for the colonization of
the islands by benthic marine species.
While there have been a number of
previous studies on the fauna associated
with the rocky shores, or with littoral and
infralittoral algae (e.g. Hawkins et al.,
1990; Bullock et al., 1990; Bullock, 1995;
taxa reviewed by Morton & Britton, 2000),
and which have normally been taxon specific (see papers by Chapman et auctt. in
Morton, 1990), there have been few published studies of the soft-sediment communities, largely owing to their recognized sparseness. Morton (1990) points
out that there was at that time no information on the soft shores of the Azores, as
virtually all are high energy beaches,
“superficially devoid of significant life”
(see also Morton et al., 1998). Two surveys
had been conducted of the soft-sediment
fauna of the sheltered habitat within the
flooded crater of Ilhéu de Vila Franca, one
in 1988 and one in 1995 (Morton, 1990;
Wells, 1995 respectively).
During the Third International
Workshop of Malacology and Marine
Biology in the Azores in July 2006, sampling of the littoral and sublittoral softsediment benthos off Vila Franca do
Campo was undertaken in order to gain
some insight into the communities present. Some sites were sampled within the
flooded crater of the Ilhéu de Vila Franca
to compare with the findings of the 1988
and 1991 studies. Comparisons were
made between the invertebrate fauna of
quantitative (grab plus shore collected)
and qualitative (dredge) benthic samples,
as well as the fauna associated with
infralittoral algae.
2009, Sup. 6: 201-210
METHODS
Quantitative samples were collected
using a 0.025 m2 Peterson grab, taking
two replicates per sampling station.
Littoral and infralittoral sands were sampled quantitatively using a plastic scoop,
also to 0.05 m2. The samples were sieved
across a 0.5 mm mesh and sorted live.
Qualitative samples were collected
using a variety of dredges, towed at 1 to 2
knots for between 6 and 10 minutes.
Crustaceans, pycnogonids, polychaetes,
sipunculans, phoronids and echinoderms
from these samples were retained
serendipitously.
The depths of the grab and dredge
samples ranged between 12 and 250 m.
Position fixing was by GPS.
Qualitative algal samples were collected either from littoral rocks (sample
Island 24.10), or from sublittoral sites in
the crater of Ilhéu de Vila Franca.
Material as collected from the dredge
samples was also analyzed from one
SCUBA collection on algae, sponges, etc.,
at 16 m depth.
All taxa were identified to species
where possible.
Nomenclature and
authorities are as in Costello et al. (2001).
Sample numbers are prefixed “Island” for
those collected within the Ilhéu de Vila
Franca, otherwise “WVF”.
RESULTS
The sampling sites analyzed are listed
in Table 1, with depths, sampling gear
and univariate community statistics.
Quantitative samples
The twelve grab and shore-collected
quantitative samples were analyzed
together. The complete faunal data from
these samples is given in Appendix 1. It
is immediately apparent that the benthic
infauna is indeed sparse: only one of the
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL
203
TABLE 1. List of samples, with depth, sampling gear and univariate ‘community’ statistics.
Sample
Date
depth,
m
sampling
gear
WVF005
WVF006
WVF007
WVF008
WVF011
WVF015
WVF016
WVF019
WVF020
WVF021
Island24.1
Island24.2
Island24.3
Island24.4
Island24.5
Island24.6
Island24.7
Island24.9
Island24.10
WVF034
WVF035
WVF036
WVF039
WVF040
WVF041
19/7/06
19/7/06
19/7/06
19/7/06
20/7/06
21/7/06
21/7/06
21/7/06
21/7/06
21/7/06
24/7/06
24/7/06
24/7/06
24/7/06
24/7/06
24/7/06
24/7/06
24/7/06
24/7/06
25/7/06
25/7/06
25/7/06
25/7/06
26/7/06
25/7/06
42
40
178
148
16
46
19
23
50
118
0
dredge
dredge
dredge
dredge
scuba
dredge
dredge
grab
grab
grab
scoop
drift weed
scoop
weed
weed
scoop
scoop
scoop
weed scrape
grab
grab
grab
grab
dredge
dredge
0.5
0.3
0.5
0.3
0.5
0.3
0
16.7
23
36
12
38
250
species individuals
littoral/infralittoral samples contained
any macrofauna, that on the sand bar in
Ilhéu de Vila Franca (Island24.1) containing 17 individuals of the errant isopod
Eurydice affinis. Similarly, the grab samples at 12 m (WVF039) contained only a
single specimen of the bivalve Ervilia castanea. Figure 1 shows the distribution
with depth of faunal density (numbers
per 0.05 m2), number of species and
Shannon-Weiner diversity. The greatest
faunal density and number of species
occur between 20 and 40 m depth, but values are consistently low, with the average
number of species and individuals per
sample being 4.4 and 25 respectively.
7
10
10
4
26
11
8
16
7
2
1
16
25
27
3
5
8
8
1
5
6
15
12
26
6
196
17
24
91
14
2
17
129
0
719
606
0
0
0
7
12
46
105
1
20
12
species Shannon- Evenness
richness Weiner H'
2.216
2.28
0.8121
3.622
3.252
0.9788
2.762
2.887
0.8689
1.674
1.792
0.8962
4.574
3.861
0.8315
3.53
3.293
0.9518
2.203
2.772
0.924
3.325
3.033
0.7581
2.274
2.407
0.8573
3.087
2.845
0.7113
3.505
3.913
3.328
3.456
0.7259
0.7352
1.61
1.828
1.504
1.781
2.519
1.668
0.7669
0.8398
0.556
1.335
2.012
1.882
2.355
0.8106
0.9112
The community diversity is generally
low, Shannon-Weiner index values ranging between 1 and 3, and also peaks at
around 20 to 40 m depth, although, owing
to the proportionately higher number of
species (7) in a sparse fauna (n=14) at station WVF020, diversity remains in the
upper range to 50 m.
Dominant taxa were actively mobile
species, the mysid Gastrosaccus normani,
the amphipods Microdeutopus versiculatus
and Harpinia laevis, the polychaete
Armandia polyophthalma and the predatory
polychaete Glycera capitata. The most
numerous sessile species was the tubicolous polychaete Myriochele oculata,
204
A Ç O R E A N A
2009, Sup. 6: 201-210
FIGURE 1. Univariate community parameters by depth for the sedimentary infauna, quantitative
samples only.
although that species was constrained to
two stations. Indeed, of the 28 species
recorded, 21 are actively mobile species
less reliant on sedimentary-habitat stability.
Qualitative samples
The complete faunal data from the
dredge samples is given in Appendix 2.
These samples are not directly comparable as no molluscs were analyzed (they
having been removed for other studies),
and the univariate community statistics
are only indicative, as the samples were
not quantitative (although the ShannonWeiner diversity index is relatively sample-size-independent).
The fauna was again found to be
sparse and inconsistent, 29 of the 42
species recorded occurring in only one
sample. Although no dredges shallower
than 19 m were analyzed, there was an
indication that the numbers of species
and individuals were highest around 19
to 50 m depth, similar to the results from
the grab sample results, but the sample at
178 m (WVF007) had high density and
species number. Average numbers of
species and individuals were 7.5 and 16.5
respectively.
The dominant taxa were again actively mobile species, including amphipods,
decapods, errant polychaetes, while the
only obligately sessile taxa were tubicolous species, the tanaidacean Paratanais
martinsi, the spionid polychaete Spio
armata and the phoronid Phoronis muelleri,
each occurring only once.
Overall, although extra species were
found from the dredge samples (which
had taken a larger volume per sample),
the fauna was relatively similar to that
found in the grab samples.
Algal and other samples
The non-sedimentary samples were
analyzed in order to compare faunal densities and species complements of the
non-infaunal community.
Appendix 3 lists the complete faunal
data from these samples, which comprise
a scuba-collection (WVF011), floating
(Island 24.2), submerged (Island 24.4,
island 24.5) or littorally attached
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL
(Island 24.10) algae in the Ilhéu de Vila
Franca lagoon.
It is immediately apparent that the
fauna of these habitats was far denser and
more species rich. Even though the littoral
rock-pool algal sample was impoverished,
the algal samples had an average of 17
species and 360 individuals per sample.
The dominant species were the crevicial or algal-associated polychaete
Platynereis dumerilii, and peracarid crustaceans,
notably
algal-associated
amphipods (Hyale spp., Erichthonius spp.,
Microdeutopus versiculatus, Corophium acutum, Caprella acanthifera), isopods
(Dynamene bidentata, Cymodoce truncata,
Paranthura costana) and tanaidaceans
(Tanais grimaldii), together with algalassociated pycnogonids (Anoplodactylus
pygmaeus, A. angulatus) and the only
cumacean recorded during the 2006 surveys, Cumella limicola. However, other
dominant species (the polychaete Fabricia
stellata, the amphipod Dexamine spinosa)
are taxa which commonly occur in sediments, but which were not recorded away
from the algae.
Most of the species recorded from the
scuba sample, collected from 16 m depth
to the north-east off Ilhéu de Vila Franca,
were the same as those dominant taxa
from the algal samples, confirming this
dense and diverse community is not
restricted to the sheltered waters of the
crater lagoon.
DISCUSSION
The data from both sets of sedimentary infaunal samples were subjected to
multivariate analysis simply on presence
or absence of species, owing to the qualitative nature of the dredge samples. The
data set was reduced to those 30 taxa
occurring as more than one individual in
the survey, and to those samples with
some fauna.
205
The dendrogram of sample similarity
(Figure 2) shows relatively poor clustering owing to the sparse and patchy nature
of the fauna. Sample WVF040 is quite distinct, the three species recorded there
(two pycnogonids and a tanaidacean) not
being found elsewhere; this sample was
not analyzed further. Similar reasons
account for the isolation of samples
WVF007, WVF008 and Island24.1. The
remaining six grab samples and five
dredge samples show that there is, in fact,
no particular trend with depth in the
community, dredge sample WVF041,
taken at 250 m, falling comfortably within
the subcluster of four grab samples taken
at depths between 16.7 and 36 m. This
lack of a trend is confirmed by the nonparametric ordination by multidimensional scaling (MDS) (Figure 3).
Although the stations WVF007 and
WVF008, both deeper than 140 m, are isolated, the species which distinguish them,
Onuphis eremita and Ebalia tuberosa, are
not species confined to deeper water.
These results indicate an unstructured, impoverished sedimentary infauna, dominated by errant taxa which can
tolerate unstable sediments, and not wellcharacterized as a community, thus not
showing any particular community
trends with depth. This fauna is most
impoverished in shallow depths (<20 m),
where one would anticipate the greatest
degree of wave-base turbulence and thus
sediment instability. With 55 species
recorded in this limited sampling exercise, the paucity of the fauna is not a function of lack of recruitment. We may thus
attribute the impoverished sedimentary
benthos of this part of the Azores to sediment instability.
By comparison, the fauna associated
with algal habitats is both dense and
diverse. Of course, if a major route of colonization of the Azorean waters is via
drift weed, then these are the very taxa
206
A Ç O R E A N A
2009, Sup. 6: 201-210
FIGURE 2. Dendrogram by Bray-Curtis similarity (%) for sedimentary benthic infaunal samples
(presence-absence data).
which would most readily recruit. It was
notable that the densest algal-associated
communities occurred sublittorally, most
littoral algae of the adjacent São Miguel
shoreline supporting little of no fauna.
the organisation of, and inviting us to the
Workshop, and to the other participants
at the workshop for samples, assistance
with the boat-work, discussion and entertainment.
ACKNOWLEDGEMENTS
LITERATURE CITED
We are indebted to Andreia Salvador
for sampling assistance in Ilhéu de Vila
Franca, to António de Frias Martins for
BULLOCK, R.C., 1995. The distribution
of the molluscan fauna associated
with the intertidal coralline algal turf
of a partially submerged volcanic
crater, the Ilhéu de Vila Franca, São
Miguel, Azores. In: MARTINS, A.M.F.
(ed.), The Marine Fauna and Flora of the
Azores (Proceedings of the Second
International Workshop of Malacology
and Marine Biology, São Miguel, 1991).
Açoreana, Supplement [4]: 9-55.
BULLOCK, R.C., R.D. TURNER & R.A.
FRALICK, 1990. Species richness and
diversity of algal-associated micromolluscan communities from São
Miguel, Azores. In: MARTINS, A.M.F.
(ed.), The Marine Fauna and Flora of the
Azores (Proceedings of the First
International Workshop of Malacology,
FIGURE 3. MDS ordination based on the similarity data from figure 2, with circles of diameter proportional to sample depth.
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL
São Miguel, 1988).
Açoreana,
Supplement [2]: 39-58.
COSTELLO, M.J., C. EMBLOW & R.
WHITE (eds.), 2001.
European
Register of marine Species. A checklist of the marine species in Europe
and a bibliography of guides to their
identification. Patrimoines Naturels,
50: 463 pp.
GOFAS, S., 1990. The littoral Rissoidae
and Anabathridae of São Miguel,
Azores. In: MARTINS, A.M.F. (ed.),
The Marine Fauna and Flora of the
Azores (Proceedings of the First
International Workshop of Malacology,
São Miguel, 1988).
Açoreana,
Supplement [2]: 97-134.
HAWKINS, S.J., L.P. BURNAY, A. NETO,
R. TRISTÃO da CUNHA & A.M. de
FRIAS MARTINS, 1990. A description
of the zonation patterns of molluscs
and other biota on the south coast of
São Miguel, Azores. In: MARTINS,
A.M.F. (ed.), The Marine Fauna and
Flora of the Azores (Proceedings of the
First International Workshop of
Malacology, São Miguel, 1988).
Açoreana, Supplement [2]: 21-38.
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MORTON, B., 1990. The intertidal ecology of Ilhéu de Vila Franca – a
drowned volcanic crater in the
Azores. In: MARTINS, A.M.F. (ed.),
The Marine Fauna and Flora of the
Azores (Proceedings of the First
International Workshop of Malacology,
São
Miguel,
1988).
Açoreana,
Supplement [2]: 3-20.
MORTON, B. & J.C. BRITTON, 2000. The
origins of the coastal and marine flora
and
fauna
of
the
Azores.
Oceanography and Marine Biology: an
Annual Review, 38: 13-84.
MORTON, B., J.C. BRITTON & A.M.F.
MARTINS, 1998. Coastal Ecology of the
Açores, 249pp. Sociedade Afonso
Chaves, Ponta Delgada.
WELLS, F.E., 1995. An investigation of
marine invertebrate communities in
the sediments of Ilhéu de Vila Franca
off the island of São Miguel, Azores.
In: MARTINS, A.M.F. (ed.), The Marine
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(Proceedings of the Second International
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Biology, São Miguel, 1991). Açoreana,
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208
2009, Sup. 6: 201-210
A Ç O R E A N A
APPENDIX 1. Complete benthic faunal data from quantitative sedimentary samples
WVF WVF WVF Island Island Island Island Island WVF WVF WVF WVF
Sample 019
SIPUNCULA
Golfingia minuta
ANNELIDA
Glycera capitata
Glycera tesselata
Glycinde nordmanni
Eumida cf. bahusiensis
Scoloplos armiger
Spio armata
Armandia polyophthalma
Myriochele oculata
Ditrupa arietina
ARTHROPODA
Crustacea
Mysidacea
Gastrosaccus normani
Anchialina agilis
Amphipoda
Harpinia laevis
Synchelidium haplocheles
Erichthonius punctatus
Microdeutopus versiculatus
Ampithoe rubricata
Caprella penantis
Isopoda
Eurydice affinis
Decapoda
Atyaephyra desmaresti
Processa edulis
Crangon trispinosus
Parthenope expansa
MOLLUSCA
Bivalvia
Ervilia castanea
Moerella donacina
Solemya sp.
ECHINODERMATA
Echinocardium flavescens
020
021
24.1
24.3
24.6
24.7
24.9
035
036
039
2
9
3
1
6
6
22
3
1
1
1
2
42
74
4
1
1
1
2
24
7
7
4
1
22
1
4
70
3
1
1
18
8
50
2
5
14
1
5
1
33
5
1
15
1
1
1
14
5
6
1
1
2
1
1
1
17
19
1
1
1
2
1
1
2
1
1
1
1
2
1
1
7
5
1
16
91
TOTAL
2
Echinocyamus pusillus
No. of Species
No. of Individuals
034
7
14
2
2
1
17
0
0
0
0
0
0
0
0
1
4
3
3
1
6
13
10
53
10
109
1
1
28
300
BAMBER & ROBBINS: THE SOFT-SEDIMENT INFAUNA OFF SÃO MIGUEL
209
APPENDIX 2. Faunal data from qualitative dredge samples (Mollusca not included)
Sample WVF005 WVF006 WVF007 WVF008 WVF015 WVF016 WVF040 WVF041 TOTAL
SIPUNCULA
1
1
Golfingia margaritacea
1
1
Golfingia minuta
ANNELIDA
Harmothoe spp.
4
3
7
Glycera capitata
1
2
4
7
1
3
4
Glycera tesselata
1
1
Glycinde nordmanni
Nereis pelagica
3
3
Nereis diversicolor
2
2
Eulalia cf. expusilla
1
1
1
1
Spio armata
Armandia polyophthalma
1
1
Pisione remota
1
1
Onuphis eremita
6
1
7
Hyalinoecia tubicola
1
1
2
ARTHROPODA
Pycnogonida
Achelia echinata
9
9
Anoplodactylus virescens
1
1
Anoplodactylus amora
3
3
Crustacea
Mysidacea
Gastrosaccus normani
1
1
4
2
8
Amphipoda
Ampelisca spinipes
1
1
1
1
Erichthonius punctatus
Erichthonius difformis
7
1
4
12
Microdeutopus versiculatus
2
2
Melita gladiosa
2
2
Lembos websteri
1
1
Isopoda
Eurydice affinis
1
1
3
5
Tanaidacea
Paratanais martinsi
6
6
Decapoda
Processa edulis
1
2
3
Crangon trispinosus
6
6
Anapagurus laevis
1
1
1
2
3
Paguridae indet.
Galathea intermedia
1
3
4
Scyllarus arctus
1
1
Ebalia tuberosa
7
3
10
Liocarcinus arcuatus
1
1
Liocarcinus marmoreus
4
4
Liocarcinus pusillus
1
1
1
1
Pilumnoides inglei
1
1
2
Parthenope expansa
Macropodia rostrata
1
1
PHORONIDA
Phoronis muelleri
1
1
ECHINODERMATA
Echinocardium flavescens
2
2
Echinocyamus pusillus
1
1
No. of Species
No. of Individuals
7
15
10
12
10
26
4
6
10
17
8
24
5
20
6
12
42
132
210
2009, Sup. 6: 201-210
A Ç O R E A N A
APPENDIX 3. Faunal data from algal samples
Sample
SIPUNCULA
Golfingia margaritacea
ANNELIDA
Harmothoe spp.
Nereis pelagica
Platynereis dumerilii
Nainereis cf. laevigata
Euphrosyne armadillo
Polyophthalmus pictus
Eupolymnia nebulosa
Fabricia stellata
ARTHROPODA
Pycnogonida
Achelia echinata
Callipallene emaciata
Anoplodactylus amora
Anoplodactylus pygmaeus
Anoplodactylus angulatus
Crustacea
Amphipoda
Ampelisca aequicornis A
Ampelisca aequicornis B
Erichthonius punctatus
Erichthonius difformis
Microdeutopus versiculatus
Melita gladiosa
Lembos websteri
Ampithoe rubricata
Dexamine cf. spinosa
Hyale nilssoni
Hyale perieri
Corophium acutum
Caprella penantis
Caprella acanthifera
Isopoda
Paranthura costana
Eurydice affinis
Dynamene bidentata
Cymodoce truncata
Janira maculosa
Tanaidacea
Tanais grimaldii
Leptochelia caldera
Cumacea
Cumella limicola
Decapoda
Thoralus cranchi
Clibanarius erythropus
Paguridae indet.
Pilumnus hirtellus
MOLLUSCA
Gastropoda
Setia subvaricosa
Rissoa guernei
No. of Species
No. of Individuals
WVF011
Island 24.2
Island 24.4
Island 24.5
Island 24.10
1
4
2
1
162
2
129
1
2
5
1
4
12
13
6
1
6
1
5
1
9
1
2
13
4
1
47
4
1
TOTAL
7
2
351
2
1
12
1
29
5
12
0
2
15
3
3
12
42
26
1
4
1
8
43
51
3
3
51
37
1
13
3
12
8
1
27
9
13
31
82
7
25
85
2
4
17
55
2
21
1
18
3
11
9
22
7
7
13
5
194
15
110
2
315
17
11
11
28
1
4
2
18
1
3
1
4
7
6
22
18
38
15
8
1
4
5
2
26
196
3
3
24
140
115
4
13
25
95
184
4
57
8
56
1
4
5
2
1
5
6
1
16
129
25
719
27
606
12
1
3
7
41
1657