Marine Biodiversity Records Distribution of Lucinoma heroica

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Distribution of Lucinoma heroica (Mollusca: Bivalvia: Lucinidae) in the minimum oxygen zone in the Gulf of California, Mexico
Pablo Zamorano and Michel E. Hendrickx
Marine Biodiversity Records / Volume 5 / August 2012 / e80
DOI: 10.1017/S1755267212000644, Published online: Link to this article: http://journals.cambridge.org/abstract_S1755267212000644
How to cite this article:
Pablo Zamorano and Michel E. Hendrickx (2012). Distribution of Lucinoma heroica (Mollusca: Bivalvia: Lucinidae) in the minimum oxygen zone in the Gulf of California, Mexico. Marine Biodiversity Records,5, e80 doi:10.1017/
S1755267212000644
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Marine Biodiversity Records, page 1 of 8. # Marine Biological Association of the United Kingdom, 2012
doi:10.1017/S1755267212000644; Vol. 5; e80; 2012 Published online
Distribution of Lucinoma heroica (Mollusca:
Bivalvia: Lucinidae) in the minimum oxygen
zone in the Gulf of California, Mexico
pablo zamorano1 and michel e. hendrickx2
1
Instituto Nacional de Ecologı́a, Periférico Sur 5000, Colonia Insurgentes Cuicuilco, Delegación Coyoacán, D.F., 04530, Mexico,
Instituto de Ciencias del Mar y Limnologı́a, Universidad Nacional Autónoma de México, Mazatlán, Sinaloa, 82000, Mexico
2
From samples taken during the oceanographic cruises TALUD IV–X in the southern and central Gulf of California, Mexico,
291 specimens of Lucinoma heroica were obtained in a depth interval of 731 to 991 m. The species occurred under conditions
of severe (,0.1 ml l21O2) and moderate hypoxia (0.1 –0.5 ml l21O2). The correlation between height and length of the shell
showed isometric growth with a trimodal size distribution, showing an average interval of 3.75 mm to 47.40 mm in height and
4.96 mm to 54.00 mm in length. Small individuals (≤20 mm) were distributed in a moderate hypoxic environment, while the
larger (.35 mm) tolerated an almost anoxic habitat. Medium-sized specimens (21–35 mm) were found in concentration
close to 0.2 ml l21O2. Average density was 1.532 ind l21 in infauna samples (dredge and core) and 0.002 ind m22 in epifauna
samples (benthic sledge).
Keywords: deep-sea fauna, minimum oxygen zone, continental slope, size distribution, Gulf of California, Bivalvia, Lucinoma
Submitted 23 May 2012; accepted 24 June 2012
INTRODUCTION
Deep-sea macroinvertebrates communities are characterized
by high diversity values (Grassle, 1989; Smith et al., 1998).
In areas where the oxygen-minimum zone (OMZ) intercepts
the continental slope, anoxic and severely hypoxic benthic
fringes are species-poor, but not so hypoxic zone extending
in even deeper water which is species-rich. In the OMZ,
depth and dissolved oxygen concentration are the most
important factors affecting deep-water communities’ composition (Levin & Gage, 1998; Rogers, 2000; Hendrickx, 2001;
Levin et al., 2001; McClain, 2004; Zamorano et al., 2007a;
Hendrickx & Serrano, 2010) and species size (see Olabarria
& Thurston, 2003, 2004).
Environmental conditions occurring at bottom level in
deep sea (i.e. muddy sediments, abundant detritus as food
source, stable values of salinity and temperature) optimize
settlement and dominance of endofauna and epifauna communities which are often highly diverse (Rex et al., 2000;
Levin et al., 2001; Kröncke & Türkay, 2003; Méndez, 2007).
Deep-water crustaceans, echinoderms and fish are generally
better represented in benthic samples obtained from sledges
or beam-trawls than in box cores. Due to difficulties in operating such equipment in deep water, there is a general lack of
information related to their distribution, abundance and community composition.
On average, the continental slope descends 20 m each
1000 m (2%). Although its upper bathymetric limit varies considerably and depends essentially on the slope of the
Corresponding author:
P. Zamorano
Email: [email protected]
continental shelf, on average it extends from 200 to 2000 –
3000 m. Worldwide, the continental slope represents about
5% of the total oceanic surface, but in the exclusive economic
zone (EEZ) of Pacific Mexico it corresponds to 12.2% or
288,900 km2, regardless of the Gulf of Tehuantepec
(Longwell & Flint, 1981; Seibold & Berger, 1982; Hendrickx,
1993).
In the eastern Pacific, the upper section of the continental
slope (roughly between 100 and 1000 m) is oxygen-poor
(≤0.5 ml l21) and an OMZ has long been recognized in the
region. Worldwide, the OMZ covers an estimated area of
1,148,000.00 km2 of the ocean bottom, but nowhere is it as
extended as in the eastern Pacific. The entire Pacific coast of
Mexico, except the upper Gulf of California, is included in
the region where vertical hypoxic conditions are the most
extensive (see Dı́az & Rosenberg, 1995; Helly & Levin, 2004;
Hendrickx & Serrano, 2010).
Among the factors responsible for these phenomena, are
the reduced vertical diffusion of oxygen, the presence of
oxygen-depleted deep-water mass originating from the
North Atlantic, and the excessive consumption of oxygen in
upwelling and highly productive areas (Levin, 2002; Helly &
Levin, 2004; Hendrickx & Serrano, 2010). Along the coast of
western Mexico, these effects have been documented for the
Gulf of California, south-west Mexico and the Gulf of
Tehuantepec (Lavin et al., 1992; Lluch-Cota et al., 1997;
Hendrickx & Serrano, 2010).
The OMZ is responsible for a sharp reduction of abundance and diversity in natural communities, and represents
a physiological barrier for most species of macroinvertebrates. Consequently, there are little or no exchange
between the communities living above and below the OMZ
and their composition is generally distinct (Rosenberg et al.,
1
2
pablo zamorano and michel e. hendrickx
1983; Levin & Gage, 1998; Hendrickx, 2001; Levin et al., 2001;
Hendrickx & Serrano, 2010; Zamorano & Hendrickx, 2011).
Laboratory experiments have shown a low tolerance of
species of bivalves and echinoderms to oxygen concentrations
inferior to 1 ml21 and a correlation between oxygen concentration and maximum size of organisms (Rosenberg et al.,
1991; McClain & Rex, 2001).
Previous studies on deep-water molluscs communities in the
Gulf of California indicate that species composition and bathymetric distribution is also highly dependent on the OMZ effect
which limits colonization and affects distribution patterns
(Hendrickx et al., 1984; Rogers, 2000; Zamorano &
Hendrickx, 2009). In some cases, however, species are highly
adapted to adverse oxygenation conditions (i.e. moderate to
severe hypoxia) and dominate in habitats that would otherwise
be devoid of life (Hendrickx, 2001; Méndez, 2007; Zamorano
et al., 2007a). Common adaptations include an increase of
the branchial surface, of the respiratory rhythm and of the
capacity to remove oxygen from the environment, a better affinity of haemocyanine for oxygen coupled with a reduction of
oxygen needs, and a higher dependence on anaerobic metabolism (see Childress, 1995; Childress & Seibel, 1998; Lamont
& Gage, 2000; Levin, 2002). Lack of strong competition for
food and reduction of predator numbers also represent a significant advantage for species able to adapt to these critical conditions (Rogers, 2000; Levin, 2002).
Species of the deep-water genus Lucinoma have developed
a strong affinity for hypoxic environment via the acquisition
of bacterial chemosymbiosis that allows for oxidation of
sulphur and a reduction of oxygen-dependence (Williams
et al., 2004). Among the approximately 26 species recognized
in this genus (BSF, 2010), Lucinoma heroica (Dall, 1901)
occurs in deep water from off Santa Rosalı́a, Baja California
Sur, Mexico (Dall, 1901), to Peru (Ramirez et al., 2003;
Coan & Valentich-Scott, 2012), in depths of 730–1838 m
(Zamorano et al., 2007b). Little is known, however, about its
bathymetric and geographical distribution in the area and
its specific tolerance to oxygen-poor environment. Lucinoma
heroica (Figure 1) was found as abundant and frequent
during a series of cruises aimed at collecting deep-water
invertebrates communities along the Pacific coast of Mexico
(TALUD project) and this material is used to complete our
information on this species.
MATERIALS AND METHODS
As part of the TALUD Project (‘Bioscenosis of deep-water
fauna of the Mexican Pacific’), a total of nine cruises aboard
the RV ‘El Puma’ of the Universidad Nacional Autónoma
de México were organized in the Gulf of California, between
22o–288N and 112o–1108W, from 2000 to 2007. Samples of
the benthic macrofauna were collected in a depth-range
of 460–2309 m during the following cruises: TALUD IV,
23–27 August 2000; TALUD V, 13–18 December 2000;
TALUD VI, 13–17 March 2001; TALUD VII, 5–9 June
2001; TALUD VIII, 16–19 April 2005; TALUD IX, 10–15
November 2005; and TALUD X, 9–15 February 2007. Three
types of sampling gear were used: a benthic sledge (2.4 m
width, 0.9 m high) equipped with a modified shrimp net
(5.5 cm stretched mesh size) and an inner net of 2.0 cm
(3/4") stretched mesh size; a modified Karling dredge with a
blind back-end with capacity of 80 l of sediment; and a standard Reineck box core (42 cm by 41 cm by 59.5 cm height)
with a maximum capacity of 102 l. Volume of sediments collected with the Karling dredge and the box core were
measured and filtered through a 0.5 mm grid in order to separate the specimens of the macrofauna. The swept area
method was used to estimate the density of shells collected
with the benthic sledge, using the duration of each haul
Fig. 1. Lucinoma heroica (Dall, 1901) (EMU-6934): (A, B) right and left valves, inner view; (C, D) right and left valves, outer view. Scale bar ¼ 1 cm.
lucinoma heroica in the minimum oxygen zone
(30 minutes) and the average hauling speed (1.75 knots). All
cruises considered a total of 288 samples were taken in 127
localities using the three sampling devices: 75 with the box
core; 97 with the Karling dredge; and 116 with the benthic
sledge. Positional coordinates for each sampling station were
plotted using a GPS navigation system. Depth was measured
with an EdoWestern, analogic recorder (TALUD III –VIII)
or a SIMRAD digital recorder (TALUD IX – X). Epibenthic
water temperature and salinity were measured with a
Seabird SBE 19 conductivity – temperature –depth probe
(CTD). Dissolved oxygen content was estimated with the
Winkler method (all cruises) and with a probe attached to
the CTD (TALUD VIII –X).
The specimens of L. heroica were separated from all benthic
samples, fixed on-board with a 4% formaldehyde seawater solution, subsequently washed with tap water and preserved in
70% ethanol. Measurements (shell height (SH) in mm; shell
length (SL) in mm) were taken with a caliper (precision, +
0.005 mm) using only specimens with soft parts. A simple
linear regression analysis was used to determine the height/
length relationship. Size of each specimen was incorporated
in a frequency histogram and related to environmental conditions. Based on previous results obtained by Zamorano
et al. (2007a), depth and dissolved oxygen concentration
were selected as the most significant factors in the multiple
linear regression analysis. Results of this analysis were used
to establish the model in which shell size (y) is related to the
selected environmental factors (x1 and x2 corresponding to
oxygen concentration and depth, respectively). Parameters of
model and the model itself are described in the Results section.
The material collected during this survey is deposited in the
Regional Collection of Marine Invertebrates (EMU) of the
Instituto de Ciencias del Mar y Limnologia, UNAM, in
Mazatlan, Sinaloa, Mexico (see catalogue number in Table 1).
RESULTS
Samples of L. heroica (Dall, 1901) totalling 291 specimens
were collected in a depth-range of 731 and 991 m (Table 1).
No specimens of this species were obtained during the
TALUD VIII cruise and L. heroica was captured in 13 of the
127 localities (10.5%) where samples were obtained.
Considering all species of molluscs collected during the
survey, L. heroica was the dominant (Dm) and one of the
most frequent (F) species according to the criteria of
Glémarec (1964) and Picard (1965) in both the benthic
sledge (Dm ¼ 3.15% of individuals, F ¼ 25% of stations)
and in the sediment samples (Dm ¼ 5.4% of individuals,
F ¼ 24% of stations).
For the Gulf of California there are three previous records
of the species. The first corresponds to the type locality (Dall,
1901), off Santa Rosalia (27824′ N 111840′ W), at 1829 m; the
second (Skoglund, 2001) is located on the east side of Isla
del Carmen (25856′ N 110835′ W), between 1321 and 1334 m
depth; and the third by Skoglund (2001), near Isla San
Pedro Nolasco (27839′ N 111821′ W), between 931 and 952 m
depth.
These
earlier
records
are
located
in
the southern-central Gulf of California (Figure 2).
Unfortunately, no data related to epibenthic temperature or
oxygen concentration are available for these previous
records. In the present work, the species was collected in the
south-eastern Gulf (Figure 2), off the coast of Sinaloa and
Nayarit, and values are available for these two parameters.
All samples examined during this study were obtained in
depth ,1000 m, in an oxygen concentration range of
0.03 ml l21 to 1.03 ml l21, in moderate (.0.1 –0.3 ml l21;
97.94% of total abundance) to severe (0.03 – 0.04 ml l21;
1.72% of total abundance) hypoxia. Only one sample
(a single specimen) was collected in 926 m depth (the
deepest sampling station for the species in this survey), with
an oxygen concentration of 1.03 ml l21 (Figure 3).
The smallest and largest specimens collected measured
SH 3.75 mm, SL 4.96 mm, and SH 55.4 mm, SL 51.38 mm,
respectively. A highly significant isometric relationship
(y ¼ 0.9x – 0.96; R2 ¼ 0.990, F1, 289 ¼ 7402.62, P , 0.0000)
(Figure 4) was obtained between SH and SL for L. heroica,
thus allowing the use of any of these two parameters for
further analysis. Consequently, height was selected as the
size parameter. When samples were pooled, a trimodal
Table 1. Geographical location, environmental parameters and sampling gears used in the stations where specimens of Lucinoma heroica (Dall, 1901)
were collected during the oceanographic cruises ‘TALUD IV – XI’. Abundance refers to number of specimens per sample. DK, Karling dredge;
BS, benthic sledge; BC, standard box core. Catalogue number (EMU) is indicated for each lot.
Cruise
Station
Latitude (88 N)
Longitude
(88 W)
Depth (m)
Dissolved oxygen
concentration (ml l21)
Sampling
gear
Abundance
(L. heroica)
Catalogue
number
TALUD IV
18
25
3
25
18
25
11
25
32b
32b
17
8
14
24815′ 00′′
24851′ 42′′
22800′ 12′′
24851′ 42′′
24815′ 00′′
24851′ 42′′
23815′ 00′′
24851′ 42′′
26803′ 00′′
26803′ 00′′
25820′ 48′′
28805′ 56′′
27844′ 53′′
108817′ 06′′
108857′ 54′′
106828′ 06′′
108857′ 54′′
108817′ 06′′
108857′ 54′′
106854′ 00′′
108857′ 54′′
109855′ 24′′
109855′ 24′′
110846′ 24′′
112826′ 50′′
111836′ 58′′
926
789
731
830
920
840
785
815
865
865
836
991
924
1.030
0.290
0.120
0.130
0.290
0.220
0.150
0.040
0.100
0.100
0.030
0.264
0.197
DK
BS
BS
DK
DK
BS
BS
BS
BS
DK
BS
BS
BS
1
18
2
1
2
31
7
1
1
1
4
143
66
25
26839′ 04′′
111818′ 20′′
836
0.169
BC
13
EMU-6931
EMU-6933
EMU-6930
EMU-7068
EMU-7083
EMU-7066
EMU-6934
EMU-7067
EMU-6935
EMU-7078
EMU-6939
EMU-7537
EMU-7532
EMU-7535
EMU-7536
EMU-7533
EMU-7534
TALUD V
TALUD VI
TALUD VII
TALUD IX
TALUD X
3
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pablo zamorano and michel e. hendrickx
Fig. 2. Distribution of Lucinoma heroica (Dall, 1901) in the Gulf of California including the material collected during TALUD cruises (solid circles) and in
previous cruises (open circles). The number in parentheses indicates that the same station was sampled more than once in different cruises.
size–frequency distribution (Figure 5) was observed and
indicates the predominance of individuals with a height
between 12 and 15 mm (30% of the material collected). No
clear size distribution pattern was observed, thus indicating
that size distribution of L. heroica in the area is heterogeneous.
Of the 13 stations in which samples of L. heroica were
taken, station 8 of TALUD X cruise features the largest
number of specimens of the species (143) representing
49.3% of all specimens collected during the study.
Individuals of this sample were smaller than 17 mm in
height and present a unimodal size distribution, with 57% of
specimens between 13 and 15 mm height (Figure 6A), and
correspond to the first mode of the trimodal distribution
observed for pooled samples (Figure 5).
Station 14 of TALUD X cruise provided the second most
abundant sample, totalling 66 specimens (22.7% of the
total). However, unlike station 8 of TALUD X, the sample is
dominated by large individuals, with a mode between 34
and 46 mm, and also includes individuals as small as 9 mm
height (Figure 6B). Specimens of this sample correspond to
the third mode observed for pooled samples (Figure 5).
The analysis of a hypothetical relationship between size
distribution and oxygen concentration indicates that small
specimens (SH ≤ 20 mm) generally occur in moderate
hypoxic conditions (.0.1ml l21), while larger specimens
(SH . 35mm) are apparently able to tolerate almost anoxic
conditions (,0.1ml l21). Intermediate-size specimens (SH
20 –35 mm) were found in oxygen concentration values of
0.2 ml l21 (Figure 7).
The multivariable analysis using both environmental
factors and shell size indicates a significant value of correlation
(R ¼ 0.652) when size and oxygen concentration are compared, explaining a variance of R2 ¼ 0.425 (F1,287 ¼ 211.948;
P ¼ 0.000). When depth is also considered, correlation
increases up to R ¼ 0.704, explaining 50% of total variance
(R2 ¼ 0.496), and depth remains as a significant factor
(F2,286 ¼ 140.827; P ¼ 0.000). A regression analysis between
oxygen and depth was used to test whether there is
lucinoma heroica in the minimum oxygen zone
Fig. 3. Number of specimens of Lucinoma heroica (Dall, 1901) obtained
during the TALUD cruises in relation to oxygen concentration (histogram
obtained by the method of Sturges, 1926).
Fig. 5. Size – frequency distribution for Lucinoma heroica (Dall, 1901)
based on the specimens collected during the TALUD cruises (N ¼ 291).
Fig. 4. Linear relationship between height and length of Lucinoma heroica
(Dall, 1901) based on the specimens collected during the TALUD cruises
(N ¼ 291).
co-linearity among parameters or not. Results showed
that oxygen concentration is not a function of depth
(R2 ¼ 0.172), due to the fact that at depths greater than
700–800 m oxygen values increase steadily, corresponding to
the deepest edge of the OMZ (see Hendrickx & Serrano, 2010).
Based on the results obtained with the multivariable analysis (Table 2), the model predicting shell size (i.e. shell height)
of L. heroica as a function of depth and oxygen concentration
is defined as: y ¼ 97.770 – 126.363 oxygen – 0.051 depth. In
this model the lower the oxygen concentration the higher the
size of the specimens.
All samples considered, number of individuals of L. heroica
obtained with the Karling dredge and the box core were compared with the total volume of sediment filtered, providing an
average density of 1.532 ind. l21. Average density of L. heroica
collected with the benthic sledge and estimated with the swept
area method is 0.002 ind m22.
DISCUSSION
During the TALUD cruises L. heroica was found in samples
obtained with equipments designed to collect both epifauna
Fig. 6. Frequency histogram of size (shell height) for Lucinoma heroica (Dall,
1901) harvested at station 8 (N ¼ 143) and station 14 (N ¼ 66) during the
TALUD X cruise in the southern Gulf of California.
(benthic sledge) and endofauna (Karling dredge and box
core). Our data and the statistical analysis indicate that
L. heroica is a relatively common and dominant resident in
the OMZ, as noted by Zamorano et al. (2007a), and occurs
under severe (,0.1 ml l21O2) and moderate hypoxia (0.1 –
0.5ml l21O2). The majority of the specimens collected
5
6
pablo zamorano and michel e. hendrickx
Fig. 7. Classification of Lucinoma heroica specimens according to their size (shell height) and the dissolved oxygen concentration (ml ls21) associated with each
capture (N ¼ 291).
Table 2. Values obtained from multiple linear regression analysis for
Lucinoma heroica (Dall, 1901) in the south-central Gulf of California.
Intercept (a)
Oxygen
Depth
B
t(286)
P level
97.770
2126.363
20.051
14.915
210.320
26.366
1.312E-37
1.973E-21
7.718E-10
(97.93%), however, were associated with oxygen concentrations values comprised between 0.1 and 0.5 ml l21, which
correspond to moderately hypoxic conditions according to
the criteria of Zamorano et al. (2007a) and Hendrickx &
Serrano (2010).
The maximum size of L. heroica recorded in the literature
is 71 mm (Keen, 1971) and the size-range observed in this
study (3.75 –55.4 mm) is considerably lower. The species
was found to be recurrent in the samples taken in the
southern Gulf of California and a new upper bathymetric
limit was set at 700 m, while the lower known limit of
bathymetric distribution of this species is close to 1850 m
(Zamorano et al., 2007b). Its geographical distribution is
restricted to the central and southern Gulf of California
(Dall, 1901; Keen, 1971; Scott et al., 1990) with a single
report off the coast of Peru (Skoglund, 2001). Based on
our data, the number of localities within the Gulf of
California increased from three to 16 and it can be considered as a widespread species south of the large islands
separating the northern Gulf from the central and southern
Gulf.
Another species of the genus has been reported off the
Mexican Pacific. Lucinoma annulatum (Reeve, 1850) is distributed from Alaska to the Gulf of California, from the intertidal to 665 m (Coan & Valentich-Scott, 2012), and has been
recorded by Rı́os-Jara et al. (2008) in the continental shelf
of Jalisco and Colima, at depths of 40 –83 m. A third species
recorded in the eastern Pacific is L. aequizonatum (Stearns,
1891), known from Santa Barbara, California, and into the
Gulf of California up to Isla Santa Cruz, from 400 to 840 m
(Coan & Valentich-Scott, 2012). Unfortunately, there are no
data related to the density or their affinity with the OMZ for
any of these two species, thus making comparison with our
results impossible.
According to Hendrickx & Serrano (2010), the OMZ in the
central and southern Gulf of California extends from 75–150 m
(upper limit) to 700–800 m (lower limit), depending upon the
latitude. Below this lower depth limit, oxygen concentration
gradually increases and reaches values .2.0 ml l21 in the
2000–2500 m depth-range (Hendrickx, 2012). The absence of
L. heroica in water deeper than 991 m (i.e. with higher
oxygen content) during the TALUD survey indicates that it is
restricted to the area where oxygen concentrations are low.
This is certainly related to its capability to survive in adverse
conditions using the chemosymbiosis processes that allows
for a reduction of oxygen-dependence, and to the fact that
Lucinoidae are considered the most diverse group of chemosymbiotic molluscs (Dando et al., 1986; Taylor & Glover, 2006).
Depth and oxygen concentration seem to be critical factors
regarding size distribution in L. heroica, with smaller specimens found in deeper water and in increasing oxygen
content compared to larger specimens. However, further
data are needed to confirm this trend.
ACKNOWLEDGEMENTS
The authors thank the participants in the TALUD cruises for
their support provided during the oceanographic campaigns
aboard the RV ‘El Puma’. P.Z. thanks José Salgado and Soledad
Ibarra for their support in the laboratory. Part of this study
was supported by CONACyT (project 31805-N) and DGAPA,
UNAM (project IN-217306-3). Ship time was granted by
UNAM (Coordination of Scientific Research). We also thank
José Salgado Barragán for his technical assistance with preparing
and editing Figure 1. P.Z. was supported by the Graduate
Scholarship Program from CONACyT (number 190220).
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Correspondence should be adressed to:
P. Zamorano
Departamento de Ecologı́a de Comunidades
Instituto Nacional de Ecologı́a
Periférico Sur 5000, Colonia Insurgentes Cuicuilco
Delegación Coyoacán, Mexico, D.F. 04530
email: [email protected]