14arine Environmental Research 16 (1985) 231-242
Meiofauna and Chlorophyll Associated with Beggiatoa
Mats of a Natural Submarine Petroleum Seep
Paul A. Montagna & Robert B. Spies
Environmental Sciences Division,
Lawrence Livermore National Laboratory, University of California,
PO Box 5507, L-453, Livermore, California 94550, USA
(Received: 12 April, 1985)
ABSTRACT
Previous studies at the Isla Vista oil seep have suggested that meiofauna,
particularly nematodes, might be an important factor in explaining
macrofaunal enrichment by making bacterial biomass available to the
benthic food web. To explore this possibility, we analyzed meiofaunal
abundance and microalgal pigments inside and just outside oJ"bacterial
mats at this natural oil seep.
The bacterial mats occur where crude oil and natural gas are actively
seeping out of the sediment; cores from within the mats contained a great
deal of crude oil (up to 50 %). Meiofaunal abundances were the same in
and out of the bacterial mats (averaging 1"9 × 106 individuals m-2).
However, dramatic changes in community structure were noticed.
Harpacticoids made up 19% of the fauna outside the mats but only 1%
inside. Pigment concentrations were also the same in both sites with
phaeophytin dominating chlorophyll (120 compared to 29.8mg m-2).
The variance of both microalgal pigments and meiofauna was much
greater inside than outside, suggesting that the bacterial mats are a more
heterogeneous environment.
Although the effect of crude oil toxicity is not clear, the high
abundances of microbial and meiofaunal biomass support the hypothesis
of benthic enrichment via microbes and meiofauna.
INTRODUCTION
Natural petroleum seepage is estimated to contribute 10 % of the total
hydrocarbons entering the oceans annually (Wilson et al., 1974; National
231
Marine Environ. Res. 0141-1136/85/$03"30 ~ Elsevier Applied Science Publishers Ltd,
England, 1985. Printed in Great Britain
232
Paul ,4. :tIontagna, Robert B. Spies
Academy of Sciences, 1975). The fault-riddled southern California
continental borderland has more than 2000 seeps, and seepage from the
Coal Oil Point region is the most active known in the world (Allen et al.,
1970; Fisher, 1978).
The Isla Vista seep, in the Coal Oil Point region of the Santa Barbara
Channel, has recently been the subject of intense study. This seep
possesses a heterogeneous distribution of hydrocarbon composition and
concentration (Stuermer et al., 1982). The macrofauna of the seep, which
is dominated by deposit-feeders, have higher densities than a nearby
nonseep site (Spies & Davis, 1979; Davis & Spies, 1980).
Bacterial mats of Beggiatoa are associated with active seepage (Spies et
al., 1980). Organic-enrichment, via hydrocarbon-degrading and sulfideoxidizing microbes, has been hypothesized to explain the high faunal
densities at the seep site (Spies et al., 1980). Recent evidence suggests
meiofauna are central to the enrichment hypothesis. Isotopic ratios of
sulfur and carbon are consistent with a trophic pathway of petroleum
energy from sulfate reducers to H2S to Beggiatoa to nematodes and to
other infauna (Spies & Des Marais, 1983). Because meiofauna are known
to have close trophic links to bacteria in general (Coull, 1973: Gerlach,
1978; Tietjen, 1980; Kuipers et al., 1981), it seems important to initiate
studies of meiofauna associated with oil seeps.
This introductory study was designed to investigate links between
meiofauna, and microbial mats of oil seeps. Because many studies have
demonstrated toxic effects of oil on meiofauna, the first question of
interest is: Do meiofauna exist in these areas of actively seeping oil? If
meiofauna are present, are they abundant enough to support dynamic
trophic processes? Since microphytobenthos are important sources of
food to meiofauna (Admiraal et al., 1983; Montagna, 1984), are benthic
algae associated with the microbial mats? Beggiatoa mats represent the
largest concentrations of bacteria at the seeps and are associated with
active seepage, so samples were taken inside and outside the mats. We
measured the microalgal pigments and meiofaunal abundance and
identified the harpacticoid population structure.
MATERIALS A N D M E T H O D S
Sampling was performed by divers at a seep 300 m offshore of Isla Vista,
California, USA. The seep is located on a fine-sand bottom at 15 m depth
Meiofauna and chlorophyll at a natural petroleum seep
233
(Spies & Davis, 1979). Beggiatoa mats are not always present, and they
depend on relatively quiet waters (R. B. Spies, pets. obs.). Therefore,
sampling was carried out in the fall (21 September, 1983) before winter
storms. The mats are white and cover areas where oil is actively seeping
out of the bottom (see Spies & Davis, 1979, and Spies et al., 1980, for
photographs of Beggiatoa and mats). Samples were taken both inside and
outside of the mats. For meiofauna, cores (50 cm 3 syringes with bottoms
cut off and a cross-section 5-5 cm 2) were taken to a depth of 5 cm. For
pigments, cores (5cm 3 syringes with bottoms cut off, yielding 1.1 cm z
samples) were taken to a depth o f 1 cm.
Meiofauna were extracted by the decantation technique, counted to
major taxa, and the harpacticoid copepods identified. The samples from
within the mats contained a great deal of oil (up to 1 0 ~ ) and required
special processing. Water was added to the sample (5:1), which was then
vigorously stirred. The oil phase separated after a few minutes and was
removed. No meiofauna are found in the oil fractions of test samples, so
thi's layer was discarded. It was sometimes necessary to repeat this
procedure three or four times to remove all of the oil.
t
Z
O3
~\
0
INSIDE MAT
m
I.-._I
/
..~_~..,jv._J
~J'\",,.._ ..~
550
Fig. 1.
600
,
CRUDE OIL
650
700
WAVELENGTH
750
800
Relative spectrophotometric absorbance of acetone extracts of samples from
inside and outside bacterial mats and of a crude oil sample.
234
Paul A. Montagna, Robert B. Spies
The sediment samples for the pigment analyses were immediately
placed on dry ice in the field and stored for four weeks at - 3 8 ° C . In
addition to preservation, freezing enhances the extraction (American
Public Health Association, 1971). The sediment samples were ground for
I min, then pigments were extracted for 24 h in 90 ~o acetone at 4 °C in the
dark. Acetone is a more efficient solvent than methanol when extracting
chlorophyll from sediment samples for spectrophotometry than methanol (Brown et al., 1981). The concentration of chlorophyll-a was
determined by spectrophotometry and the phaeophytin-a concentration
was determined spectrophotometrically after acidification (Lorenzen,
1967). The presence of oil in the mat samples required two special
modifications. Oil absorbs strongly between 340 and 500nm, with an
additional peak at 571 nm (Fig. I). However, past 600nm the baseline for
crude oil was flat. Therefore, centrifugation for 10 min at 500 g (to remove
particulate interference) and readings at 750 nm (to subtract sediment oil
background) were used to measure pigment absorbance. A second
interference by oil was found upon acidification. Addition of acid at high
concentration (0.1 M) increased absorbance in the samples containing oil.
But this interference subsided when acid at low concentration (0.003 ~)
was added as suggested by Riemann (1978).
Data were analyzed using B M D P software (Dixon, 1983). The t-test
was used for meiofauna data (program P3D). Much more complicated
analyses were required for the pigment data. The problem is like a twoway analysis of variance (ANOVA): site (in or out of mat) versus pigment
TABLE 1
Concentrations of Microalgal Pigments, Determined by
Spectrophotometry, from Inside and Outside Beggiatoa Mats
Mat site
Sediment
core
Pigment measurements
(mg m - 2)
Chlorophyll-a
Out
Out
Out
In
In
In
1
2
3
4
5
6
43-1
32-9
32-6
25.3
16.6
28.0
Phaeophytin-a
117
1t I
94-0
124
170
107
235
Meiofauna and chlorophyll at a natural petroleum seep
(chlorophyll or phaeophytin). But phaeophytin is determined after
acidification of the same sample from which chlorophyll is measured;
thus the pigments are a repeated measure from each core sample and
each core comes from only one site. That is, cores are nested even
though the pigments are crossed. This is a completely random and
partially hierarchical design (Kirk, 1982, p.470). The appropriate
statistical model is
Yijk =
'~ i -4;-~j(i) "~- 7k "~- ~ ik AV ( ~
)j(iJk
where the variation of each measurement Y,~kis a function of ai (a site
effect), sediment core flJ(o (a nested effect), pigment '/k (a crossed effect)
and interaction terms. Program P2V was used for this analysis.
RESULTS
The oil seep area is a curious place. Gas bubbles and oil droplets rise to the
surface and form oil slicks. Beggiatoa mats occur directly over active
seepage; thus cores through the mats contain large quantities of oil. One
might imagine that nothing could live there at all. This environment does
appear to stress microalgae. Phaeophytin concentrations are 4 x greater
than chlorophyll (Table 1): P = 0 - 0 0 1 4 (Table 2). It is reasonable to
hypothesize that chlorophyll would be favored outside the mat and
phaeophytin inside the oiled mat, thereby yielding a significant
interaction term. Although the data suggest that phaeophytin is more
abundant in the mat (the mean, Z = 134 mg m - 2 ; standard deviation,
TABLE 2
Analysis of Pigment Data (Table 1) Using a Partially Heirarchical
Model
(Numerator and denominator used in F-test is shown in brackets)
Source
1
2
3
4
5
A(site)
B(A)(core)
C (pigment)
A x C
B(A)×C
df
SS
F
P
1
4
1
1
4
135
990
24707
1 154
1561
[I/2] 0-55
[2/5] 0.63
[3/5]63-29
[4/'5] 2.96
0-5507
0.7000
0-001 4
0-1606
Paul A. Montagna, Robert B. Spies
236
s = 33) than outside ( X = 107mg m - 2 s = 12) and chlorophyll is more
a b u n d a n t outside ( X = 36"2 mg m--' s = 6.0) than inside ( X = 23-3 mg
m--', s = 6"0), the interaction term was not statistically significant
(P = 0" 16; Table 2). The lack of significant interaction is probably due to
the small numbers of samples and the large variance associated with
phaeophytin concentrations, particularly those inside the mat (Table 1).
Meiofaunal populations also exhibited much higher variance inside the
mat than outside (Table 3; P = 0.0202). The abundances of meiofauna
TABLE 3
Meiofaunal Population Abundances Inside and Outside of the Oil Seep Beggiatoa Mats
( × 103 individuals m -z)
Site
Out
Out
Out
Out
Out
In
In
In
In
In
Sample Totals
I
2
3
4
5
1
2
3
4
5
1880
2960
1880
2500
3040
662
337
3 170
511
2290
Nematodes Copepods Naupli Oligochetes Ciliates Others ~
1200
2360
1340
1860
1800
632
326
3070
49l
2 230
448
406
355
342
821
7
5
26
5
0
49
55
51
73
129
0
0
0
0
0
62
20
0
1l
33
16
4
9
13
5
58
76
86
122
191
4
2
60
2
53
64
47
45
91
65
4
0
5
0
4
~Cumacea, Ostracoda Cipriids, Isopoda, Halacarida, Ophiuroidea larvae, larval
Pelecypoda, Gastrotricha, Turbellaria and Foraminifera.
were not significantly greater (t-test; P = 0. 1259) outside the mat ( X =
2.45 × 106 individuals m -2, s = 0.56 x 106) than inside ( X = 1.39 × 106
individuals m -2, s = 1-26 x 106). More taxa were found outside than
inside. Whereas all of these t a x a - - C u m a c e a , Ostracoda Cipriids,
Isopoda, Halacarida, Ophiuroidea larvae, larval Pelecypoda, Gastrotrichia, Turbellaria and Foraminifera--were present outside, only
a single ostracod or foraminiferan plus several ciprid larvae were found
inside the mats. Many larger oligochetes and polychetes were present
(Spies & Davis, 1979; Davis & Spies, 1980) but were not o f a meiofaunal
size.
The harpacticoid copepods were very diverse and a b u n d a n t at the oil
seep site (Table 4). Just outside the mat there were 34 species compared to
four inside, with two species occurring in both locations.
)Ieiofauna and chlorophyll at a natural petroleum seep
237
TABLE 4
Copepod Species Abundances Inside and Outside of Oil Seep Beggiatoa Mats
(mean number of individuals ( + standard deviation) 10 cm - 2)
Family
Longipedidae
Ectinosomatidae
Harpacticidae
Tisbidae
Thalest ridae
Diosaccidae
Ameiridae
Cletodidae
Canthocamptidae
Loaphontidae
Anacorabolidae
Total
Species
Longipedia (cf.) minor
Ectinosoma paranormani
Ectinosoma melaniceps
Halectinosoma kunzi
Microsettella norvegica
Pseudobradya pectinifera
Pseudobradya crassipes
Zausodes sextus
Zausodes septimus
Tisbe sp.
Dactylopodia paratisboides
Diarthrodes dissimilis
Amphiascoides lancisetiger
Amphiascoides petkocskii
Diosaccus spinatus
Robertgurnea diL'ersa
Robertsonia propinqua
Stenhelia (D.) (cf.) hanstromi
Stenhelia (D.) Iongipilosa
Stenhelia (S.) peniculata
Stenhelia (S.) proxima
Tyhplamphiascus sp.
Pseudoamphiascus sp.
Ameira parvuloides
Ameiropsis sp.
Leptomesochra sp.
Acrenhydrosoma karl#tga
Cletodes hartmannae
Enhydrosoma hopkinsi
Stylicletodes cerisimilis
Orthop©'llus illgi
Normanella bolini
Normanella con[tuens
Paralaophonte asellopsiformis
Paralaophonte pac(fica
Laophontodes hedgpethi
Outside
Inside
10.9 (6"2)
10.6 (7.9)
07 (1'0)
2-0 (3"2)
0-7 (1'0)
0.4 (0"8)
1"1 (l'0)
138.0 (55.9)
4 4 (7-9)
7.3 (9.4)
28.4 ( 16-1)
37-1 (27.3)
29.5 (22.0)
2.9 (6.5)
0.4 (0'8)
269 (14.8)
2.5 (2.8)
31.3 (I 1.2)
0-4 (0.8)
0-7 (l'0)
0.4 (0-8)
14.6 (4.6)
1.4 (2.4)
15-7 (9"8)
0.7 (I.0)
1.1 (I.6)
1.8 (2-2)
0.7 (1.6)
7-3 (6-4)
0 4 (0-8)
2-5 (3'0)
58"2 (31.4)
14.6 (4-5)
16.7 ( 1 1.5)
2.9 (28)
0-4 (0"8)
466
0.4(0.8)
0-4(0.8)
9-5
238
Paul A. Montagna, Robert B. Spies
DISCUSSION
The pattern we have found is that meiofauna and chlorophyll are
predominantly associated with the fringe of the bacterial mats, not in the
center. Because the presence of mats is not constant we have not
attempted to sample more than once. But the rate o f hydrocarbon
seepage is relatively constant, so we are confident that the pattern we
describe, but not necessarily the magnitude, is representative of bacterial
mats at the oil seep. This pattern is also consistent with the finding that
A T P is most abundant at the fringes of actively seeping oil (Spies et al.,
1980). The Beggiatoa mats are found over areas of active seepage.
Beggiatoa are known to exhibit diel vertical migration in sediments in
response to light (Nelson & Castenholz, 1982). The vertical distribution
of Beggiatoa is also strongly related to the interface of oxic and anoxic
sediments (Jorgensen, 1977). We suspect Beggiatoa is always present, but
unique conditions, such as either low light conditions or lack of oxic
sediments, or both, can cause Beggiatoa to move to the surface and form
the large filamentous mats.
Whereas the bacterial mats are rich in chlorophyll-a, the dominance of
phaeophytin-a indicates microalgal populations are stressed by the
presence of crude oil, natural gas or associated sulfide (Table 1). However,
the presence of chlorophyll in the mats indicates areas of active seepage
are important potential sources of meiofaunal food because microbial
biomass is concentrated there. Although the meiofaunal populations
were not different inside and adjacent to the bacterial mats (about 1.4 and
2-5 x 106 individuals m--', respectively), c o m m u n i t y structure did shift
(Table 3).
Harpacticoids decreased dramatically from 0.474 + 0-198 to 0.009 +
0.010 x 106 individualsm -z when comparing the fringe to the center
of the mat. Therefore, harpacticoids appear to suffer stress l¥om
petroleum. Variance for all meiofaunal taxa and pigments increases at the
fringe relative to the center of the mats (Table 3). This indicates that the
center of the mats, where oil is actively seeping, is a much more
heterogeneous environment than the fringes. The fringes, which support a
rich and diverse assemblage of meiofauna (Table 4), are probably sites
where trophic-dynamic processes are carried on at peak rates. The size of
the meiofaunal population at the fringe is certainly large enough to be a
significant factor in the coastal food web. In contrast, the bacterial mat
Meiofauna and chlorophyll at a natural petroleum seep
239
(which is directly over seeping oil) is a heterogeneous environment which
appears to have limited stressful effects.
Abundances of macroinfauna at the Isla Vista oil seep are greater than
in a similar but nonseep site (Spies & Davis, 1979; Davis & Spies, 1980).
Although the details of this apparent benthic enrichment are not known,
the presence of petroleum and sulfide suggests an efficient (or
supplementary) anaerobic-based food web. This hypothesis is supported
by observations of the natural isotopic ratios of carbon and sulfur, which
suggest that sulfide is the energy source and petroleum supplies the
carbon (Spies & DesMarais, 1983).
Meiofauna appear to be the key intermediate between microbial and
infaunal biotransformations (Spies & DesMarias, 1983). Trophic enrichment associated with anaerobiosis and chemoautotrophy in sulfiderich environments appears to be a common paradigm for salt marshes
(Howarth & Teal, 1980), subsurface marine muds (Kepkay et al.,
1979), brine seeps (PoweU et al., 1983) and hydrothermal vents (Karl et
al., 1980). It appears that natural marine oil seeps can be added to this list.
Meiofauna, owing to their small size, share similar spatial and
temporal scales to microbes, particularly microalgae (Montagna et al.,
1983). As well as grazing on bacteria and benthic diatoms (Admiraal et
al., 1983; Montagna, 1984), meiofauna also appear to have roles in
biogeochemical cycles (Coull & Bell, 1979; Sikora & Sikora, 1982). So
investigating relationships between meiofauna and the sediment microbial community appears to be central to understanding the apparent
trophic enrichment in sulfide environments.
The interstitial sulfide at the Isla Vista seep is apparently of biogenic
origin (Spies & DesMarais, 1983). Large mats of the sulfide-oxidizer
Beggiatoa are found at the seep site. Blue-green algae or chlorophyll are
often associated with bacterial mats in sulfide-rich environments (Doemel
& Brock, 1976; Gallardo, 1977). These microbially-rich environments
could be an important food source to meiofauna and the center of
radiation for carbon and sulfur incorporation into the food web. Flatfish
have been seen feeding at this site by divers.
Pore-water hydrocarbon concentrations are about l ppm inside the
Beggiatoa mats and in the range of 45 to 100 parts per 109 outside
(Stuermer et al., 1982). Up to 50 ~o of the sediment sample from within the
mat can be crude oil. Thus, trophic enrichment by petroleum carbon
might be limited by the toxic effect of oil. Meiofaunal abundances,
240
Paul A. Montagna, Robert B. Spies
especially copepods, usually decrease after heavy oiling (Giere, 1979:
Bodin & Boucher, 1983). But after an experimental crude oil introduction
in Louisiana, densities did not decrease (Fleeger & Chandler, 1983).
Chlorophyll pigments also seem not to be affected by spilled oil (Bodin &
Boucher, 1983).
Whereas there are indications that natural oil seepage has some
stressful effects, the present study suggests that these effects are more than
offset by dynamic trophic processes associated with the fringes of spots of
active seepage (which are sometimes covered by bacterial mats).
Petroleum, via heterotrophic degraders, is the carbon source and sulfide,
via oxidizers, is the energy source. Meiofauna feed on both these types of
bacteria, as well as the chlorophyllous microbes (either microalgae or
cyanobacteria). This petroleum-based carbon eventually gets into the
coastal food web by macroinfaunal predation and larval fish predation on
meiofauna.
A C K N O W L E D G E M ENTS
We thank J. McCullagh for diving with us and S. Anderson of the
University of California, Santa Barbara Marine Sciences Institute, for
extensive logistical support, and F. Milanovich and L. Anspaugh for
helpful comments on the preparation of this manuscript. This work was
performed under the auspices of the US Department of Energy by
Lawrence Livermore National Laboratory under contract W-7405-Eng48.
REFERENCES
Admiraal. W., Bouman, L. A., Hoekstra, L. & Romeyn, K. (1983). Qualitative
and quantitative interactions between microphytobenthos and herbivorous
meiofauna on a brackish intertidal mudflat. Int. Revue ges. Hydrobiol., 68,
175-9 I.
Allen, A. A., Schlueter, R. S. & Mikolaj, P. G. (1970). Natural oil seepage off
Coal Oil Point, Santa Barbara, California. Science, 170, 974-7.
American Public Health Association (1971). Standard methods f o r the
examination o f water and wastewater, 13th edn, American Public Health
Assoc., New York, 746-9.
Bodin, P. & Boucher, D. (1983). Evolution a moyen terme du meiobenthos et des
pigments chlorophylliens sur quelques plages polluees par la Maree Moire
de 1"Amoco Cadiz. Oceanol. Acta, 6, 321-32.
MeioJauna and chlorophyll at a natural petroleum seep
241
Brown, k. M., Hargrave, B. T. & Mackinnon, M. D. (1981). Analysis of
chlorophyll-a in sediments by high-pressure liquid chromatography. Can. J.
Fish. Aquatic Sci.. 38, 205-14.
Coull, B. C. (1973). Estuarine meiofauna: a review: trophic relationships and
microbial interactions. I n:Estuarine microbial ecology (Stevenson. L. H. &
Colwell. R.R. (Eds)), University of South Carolina Press, Columbia,
499-51 I.
Coull, B. C. & Bell, S. S. (1979). Perspectives of marine meiofaunal ecology. In:
Ecological processes in coastal and marine systems (Livingston, R. I. (Ed.)),
Plenum Press, New York, 189-216.
Davis, P. H. & Spies, R. B. (1980). lnfaunal benthos of a natural petroleum seep:
study of community structure. Mar. Biol., 59, 31-41.
Doemel, W. N. & Brock, T. D. (1976). Vertical distribution of sulfur species in
benthic algae mats. Limnol. Oceanogr., 21,237-44.
Dixon, W. J. (Ed.) (1983). B M D P statistical soJ'tware, University of California
Press, Berkeley, 733 pp.
Fisher, P. J. (1978). Natural gas and oil seeps, Santa Barbara Basin, California.
In: The State Lands Comm. 1977, CaliJornia gas, oil and tar seeps,
California State Lands Commission, Sacramento, 1-62.
Fleeger, J. W. & Chandler, G. T. (1983). Meiofauna response to an experimental
oil spill in a Louisiana salt marsh. Mar. Ecol. Prog. Ser., 11,257-64.
Gallardo, V. A. (1977). Large benthic microbial communities in sulphide biota
under Peru-Chile subsurface counter current. Nature, 268, 331-2.
Gerlach, S. A. (1978). Food-chain relationships in subtidal silty sand marine
sediments and the role of meiofauna in stimulating bacterial productivity.
Oecologia, 33, 55-69.
Giere, O. (1979). The impact of oil on pollution on intertidal meiofauna. Field
studies after the LA CORUNA spill, May 1976. Cah. Biol. Mar., 20,
231-51.
Howarth, R. W. & Teal, J. M. (1980). Energy flow in a salt marsh ecosystem: the
role of reduced inorganic sulfur compounds. Am. Nat., 116, 862-72.
Jorgensen, B. B. (1977). Distribution of colorless sulfur bacteria (Beggiatoa spp.)
in a coastal marine sediment. Mar. Biol., 41, 19-28.
Karl. D. M., Wirsen, C. O. & Jannasch, H. W. (1980). Deep sea primary
production at the Galapagos hydrothermal vents. Science, 207, 1345-7.
Kepkay, P. E., Cooke, R. C. & Novitsky, J. A. (1979). Microbial autotrophy: a
primary source of organic carbon in marine sediments. Science, 204.68-9.
Kirk, R. E. (1982). Experimental design, 2nd edn, Brooks/Cole Publ. Co.,
Monterey, CA, 911 pp.
Kuipers, B. R., de Wilde, P. A. W. J. & Creutzberg, F. (1981). Energy flow in a
tidal flat ecosystem. Mar. Ecol. Prog. Ser., 5, 215-21.
Lorenzen, C. J. (1967). Determination of chlorophyll and phaeo-pigments:
spectrophotometric equations. LimnoL Oceanogr., 12, 343-6.
Montagna, P. A. (1984), In situ measurement of meiobenthic grazing rates on
sediment bacteria and edaphic diatoms. Mar. Ecol. Prog. Set., 18, 119-30.
Montagna, P. A., Coull, B. C., Herring, T. L. & Dudley, B. W. (1983). The
242
Paul A. Montagna, Robert B. Spies
relationship between abundances of meiofauna and their suspected
microbial food (diatoms and bacteria). Estuar. Coast. Shelf!Sci., 17,381-94.
National Academy of Sciences (1975). Petroleum in the marine environment.
Workshop on inputs, fates and effects of petroleum in the marine
environment. National Academy of Sciences, Washington, DC, 107 pp.
Nelson, D. G. & Castenholz, R. W. (1982). Light responses of Beggiatoa. Arch.
Microbiol., 131, 146-55.
Powell, E. N., Bright, T. J., Woods, A. & Gittings, S. (1983). Meiofauna and the
thiobiosis in the East Flower Garden brine seep. Mar. Biol., 73, 269-83.
Riemann, B. (1978). Carotenoid interference in the spectrophotometric determinations of chlorophyll degradation products from natural populations of
phytoplankton. Limnol. Oceanogr., 23, 1059-2066.
Sikora, W. B. & Sikora, J. P. (1982). Ecological implications of the vertical
distribution of meiofauna in salt marsh sediments. In: Estuarine
comparisons (Kennedy, V. S. (Ed.)), Academic Press, New York, 269-82.
Spies, R. B. & Davis, P. H. (1979). The infaunal benthos of a natural oil seep in
the Santa Barbara Channel. Mar. Biol., 50, 227-37.
Spies, R. B. & DesMarais, D. J. (1983). Natural isotope study of trophic
enrichment of marine benthic communities by petroleum seepage. Mar.
Biol., 73, 67-71.
Spies, R. B., Davis, P. H. & Stuermer, D. H. (1980). Ecology of a submarine
petroleum seep off the California coast. In: Marine environmentalpollution.
1. Hydrocarbons (Geyer, R. A. (Ed.)), Elsevier Sci. Publ. Co., Amsterdam,
229 -63.
Stuermer, D. H., Spies, R. B., Davis, P. H., Ng, D. J., Morris, C. J. & Neal, S.
(1982). The hydrocarbons in the Isla Vista marine seep environment. Mar.
Chem., 11,413-26.
Tietjen, J. H. (1980). Microbial-meiofaunal interrelationships: a review.
Microbiology 1980, 335-8.
Wilson, R. D., Monaghan, P. H., Osanik, A., Price, L. C. & Rogers, M. A.
(1974). Natural marine oil seepage. Science, 184, 857-65,