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The ecophysiology of some marine nematodes from Bermuda: Seasonal aspects
J. exp. mzr.
Biol. Ecol.,
Q Elsevier/North-Holland
1977, Vol. 26, pp. 97-106;
Biomedical Press
THE ECOPHYSIOLOGY
OF SOME MARINE NEMATODES
BERMUDA:
SEASONAL
FROM
ASPECTS
WOLFGANG WIESER Institut fiir Zoophysiologie
der Unioersitiit,
Innsbruck,
osterreich
and FRITZ SCHIEMER Lehrkanzel
fiir Limnologie
der Uniuersitiit,
Wien, i)sterreich
Abstract: In the winter of 1976 the horizontal and vertical distribution, temperature tolerance, and oxygen consumption at three experimental temperatures were determined for several species of nematodes inhabiting a low-energy beach in Bermuda. The results are compared with those of previous summer investigations carried out on the same beach. The three most abundant species of nematodes on the beach, Steineria sterreri Ott, Trefitsia schiemeri Ott and Theristllsfloridunus Wieser & Hopper show distinct patterns of distribution as well as distinct survival-time curves when upper lethal temperature is plotted against exposure time. No seasonal resistance adaptation to high temperature occurs in Steineriu sterreri and Trefusia schiemeri, the two species for which comparative summer data are available. Theristus erectas, which dominated the flat in summer, is much more heat tolerant than T.Jloridanus which replaced it in winter. Oxygen consumption at 15 “C is twice as high in T. ,jforidanus as in Trejiisiu schiemeri, whereas at 22 ’ and 30 “C both species consume approximately the same amount of oxygen. T. schiemeri is capable of seasonal adaptation of Qo, inasmuch as it consumes just about as much oxygen in winter at 22 “C as in summer at 30 “C. The seasonal data support the suggestion that on a subtropical low-energy beach the metabolic capacities of many meiofauna species are closely adjusted to the micro-environment in which they live.
An earlier investigation
into the ecophysiology
of the meiofauna
inhabiting
a sub-
tropical beach in Bermuda (Wieser et al., 1974; Wieser, 1975) led to the conclusion that the upper lethal temperatures and pH values of most of the species studied are closely related to their vertical distribution
in the sediment
as well as to the maximum
values of temperature and pH measured at the centre of distribution of each species, and that there is a relation between the respiratory rates of nematodes and their vertical distribution in the sediment. Furthermore, the acclimation of nematodes to different environmental temperatures has no effect on their oxygen consumption measured at 30 “C. It is of interest to determine whether season has any effect on these relations which were established during the summer. For example, if it were generally 1 Contribution
No. 683 from the Bermuda Biological Station for Research. 97
WOLFGANG
98
WIESER AND FRITZ SCHIEMER
true that the upper lethal temperatures &he maximum
temperatures
lower vaIues of LT,, “resistance adaptation”
of marine
experienced
in winter
than
meiofauna
in their habitats, in summer,
species are very close to one would
i.e., a considerable
expect much amount
in the sense of Precht (1955, 1958). In order to consider
and some related problems
an investigation
of selected nematode
Town Cove Beach was carried out in February MATERIAL AND
of this
species from Tuckers
1976.
METHODS
AREA OF THE INVESTIGATION
Field measurements and sampling were carried out at Tuckers Town Cove Beach, Bermuda. The locality has been described briefly by Wieser ef al. (1974) and by Wieser & Zech (1976). A thorough analysis of the IocaIity has more recently been completed by Farris (1976) and it is simplest to quote the following facts which are pertinent to our study. “Tuckers Town Cove Beach is Iocated in Tucker’s Town Bay on the SW side of Castle Harbour . . ,. A perpendicular bar extends across the beach 62 m from spring high tide Ievel (S.H.T.L.). The bar restricts water movement along the landward side of the beach at low tide. Mean slope of the beach to the bar is approximately 1.5 % with the greatest decline occurring in the first 13 m from S.H.T.L. Seaward from the bar, the beach slopes on an average of 4 % descending subiittorally into a deep channel. Tidal ranges seldom exceed I m vertically and 85 m horizontally. Sand is calcareouswith a mean grain size of 250 pm (4 2) . . . Stands of red mangroves (Rhizophora mangle) lie adjacent to the beach on the northwest side and contribute heavily to organic matter in the beach ecosystem. The reducing nature of TTCB is particularly evident during low tide at which time the odor of hydrogen sulfide can be detected.” sediments
Perhaps it should be pointed out that for a marine ecoIogist used to silicate in temperate regions, this beach is unusual insofar as it consists of medium-
sized, well sorted sand of the type one would expect on a high-energy
beach, whereas
its rich content
only a few mm
of organic
below the surface indicate
matter
as well as a reducing
a low-energy
environment
beach.
SAMPLES
Samples were taken at Iow tide at three sites along an east-west transect across the intertidal beach, above and below mean water leve1 (Fig. 1). Cores with a cross section of 10 cm2 were taken and sectioned to give the following vertical zones: O-l, 1-2, 2-5, 5-10 cm. For the experiments animals were separated from bulk samples by the usual shaking and decanting procedure. The water content of aliquot sediment samples from the top 1 cm layer was determined by weighing and drying at 100 “C. Redox potentials were measured with a Corning portable voltmeter using a platinum electrode and a Corning calomel reference electrode. Temperature was measured with a mercury thermometer.
ECOPHYSIOLOGY
OF SOME
MARINE
NEMATODES
99
SPECIES
The following species of nematodes were studied: Trefusia schiemeri Ott (in press) 1 Tripyloides n.sp. in Wieser et al. (1974) and Wieser (1975); Theristars Jloridanus Wieser & Hopper (1967); ~~~~~e~~a sterreri Ott (in press) = Steineri n.sp. in Wieser (1975); and Paramonhystera wieseri Ott (in press) = Paramonhystera n.sp. in Wieser et al. (1974) and Wieser (1975). SURVIVAL
EXPERIMENTS
In order to establish upper lethal temperatures groups of animals (mostly 20 to 30, sometimes only 10) were put into filtered, normoxic sea water in small vials. The stoppered vials were submerged in a water bath and subjected to high temperatures for 1 to 10 h. Results are expressed as LTSO, determined from the regression lines of temperature on survival (see Wieser et al., 1974). OXYGEN CONSUMPTION
Adult males of two of the species studied were separated (shaking and decantingtechnique) from large samples of sand usually taken within 24 h before the experiments. Before sorting, the samples were stored in the laboratory at x 20 “C. The experimental animals were held in filtered sea water, containing 1000 I.U. of streptomycin and 1000 I.U. of penicillin per ml at the experimental temperature for 1 h. The oxygen consumptions of individual animals was measured using ‘stoppered Cartesian divers’ (0.5-1.5 ~1) as described in detail by Klekowski (197l),at 15 O,22 ‘, and 30 “C. The divers were filled with sea water filtered through a 0.45 pm Millipore filter and re-aerated. The animals were positioned in the divers by means of capillary pipettes. After loading, the divers were put into the flotationvessels and the equilibrium pressure was roughly adjusted. Manometric reading started 1 h later and lasted 3-6 h. Experiments giving readings which were not linear with time were discarded. Control runs were carried out at each experimental temperature in order to check the thermostability of the water-bath and to establish the equilibrium time required for each experimental temperature. Camera-lucida drawings were used to calculate the volumes of the experimental animals. Weight-specific respiratory rates in ~1 O2 mg-” h-’ are based on these volume determinations, assuming a specific gravity of 1.00.
RESULTS TEMPERATURE
According to the records kept at the Bermuda Biological Station the following ranges of temperature (“C) prevailed in the months December, 1975 to February,
WOLFGANG
100
1976 (the water temperature Reach and the air temperature
WIESER AND FRITZ SCHIEMER
was measured off the dock of the Biostation at Ferry at the dock, both in the morning).
December Maximum “C Minimum “C
Water 20.8 17.2
January
February
Air
Water
Air
Water
Air
21.6 16.1
18.6 16.1
21.1 14.4
18.8 16.4
22.1 13.1
At Tuckers Town Cove Beach at low tide the water remaining on the flat and in tidal pools might warm up several degrees above the temperature of the offshore water. During the period of our work (4th-25th Feb.) we recorded maximum water temperatures on the flat of 26 “C, maximum surface temperatures of exposed sand of 24.5 “C: values as high as these occurred, however, only on a few days at noon. Usually, the temperature of the sand surface at low tide varied between 16 ’ and 23 “C. Minimum values measured on the sand surface were 12.5 * to 13 “C. REDOX POTENTfALS
Several series of Eh measurements were carried out at the three sites. The ranges of Eh values recorded, from the surface to 10 cm depth, are given in Fig. 2. The bar sand remains oxygenated down to the greatest depth measured, whereas on the flat the sediment is highly reduced below 1 cm. The shoulder site occupies an intermediate position with the redox discontinuity layer situated between I and 2 cm. These differences in the degree of reduction of the sediment between the three sites are closely correlated with their elevation above low-tide level and with the water content of the sand (Fig. I). The higher the site above the low tide level, the more unsaturated is the top layer and the more oxygenated are the lower layers of the sediment core. DISTRIBUTION
OF NEMATODES
Samples were taken at three sites on the beach, namely ‘bar’, ‘shoulder’ and ‘flat’. The position of these along an east-west transect of the beach, the water content of the top layer of sediment at low tide, as well as the abundance (per 10 cm3 wet sediment) of the three dominant species of nematodes found at these sites are summarized in Fig. 1. The ‘bar’ site is clearly dominated by Stein&a sterreri, with very few other species of nematodes present. The ‘shoulder’ site is characterized by the dominance of Trefusiu schiemeri: many other species of nematodes are present but none in comparable numbers. The surface tayer of this site also has abundant harpacticoids, probably belonging to the species studied in 1973, i.e., Roberfsonia lcnoxi (Thompson & A. Scott), Amphia~co~de~ ~~bdebii~~ (Willey) and Ps~~~ocarnp~s nsp. (see Wieser et al., 1974). The ‘flat’ site is richest in nematode species and the dominance of Ther~~t~s~oridon~~ is not as striking as that of Steineria sterreri and Trefusia s~t~~e~~eri
ECOPHYSIOLOGY
at the other two sites. The anaerobic occurs in moderate
numbers
East
OF SOME
MARINE
species Paramonhystera wieseri, studied in 1973,
below 2 cm both at the shoulder
bar
HWL
0
101
NEMATODES
shoulder @
and at the flat site. West ,m 1.0
________---------
p 40 m
0.8 i% 0.6 ” z 0.4 m
20 aI” 30 0, 10
0.2
Fig. 1. An east-wast profile of Tuckers Town Cove Beach, Bermuda, showing thz three sampling sites: bar (I), shoulder (2), and flat (3): upper graph shows water content (g water/g wet sediment weight x 100) of the uppx cm of sand at four points along the transect: lower graph gives the abundance (individuals/lo cm3 sediment) of three dominant species of nematodes at the three sampling sites: Sst., Steineria sterreri; T.s., Trefuria schiemzri: Th.f., Theristus fioridanus; HWL, mean high water level; LWL, mean low water level.
Steineria, Trefusia, and Paramonhystera have been found
at this beach regularly
since the summer of 1973 when our research started. Theristusjoridanus, however, is a newcomer to this locality. Although one of the most frequent inhabitants of shallowwater sediments in the area, particularly in Caste1 Harbor at 3 m depth (Coull, 1968), it had not been found previously on Tuckers Town Cove Beach. In 1973, the upper sediment layers of the flat were dominated by T. erectus (Wieser & Hopper, 1967). In the summers of 1974 and 1975, Theristus sp. seemed to have become scarce but no detailed analysis of its distribution was made at those times. In February 1976, T. erectus had definitely
disappeared
and T. floridanus made its appearance.
Vertical distribution The vertical distribution of the three nematode species dominating the three sites, as well as that of Paramonhystera wieseri, is summarized in Fig. 2. The vertical and horizontal patterns of distribution are distinct and may serve to characterize the three sites studied. Trefusia schiemeri, so abundant in the upper 2 cm of the shoulder site, does not occupy this zone to any noteworthy degree on the flat, but finds its centre of abundance there below a depth of 2 cm. This maybe the result of competition with Theristus joridanus which appears to be the more successful surface species in the flat, the less successful one on the shoulder. The distribution of Paramonhystera wieseri is clearly correlated with the occurrence of reducing conditions in the sediment.
WOLFGANG
102
WESER
AND FRITZ SCHIEMER
i
o-21-
-__i-Le.t
13
5
7
9 haursexposura
7
9
Fig, 3. Upper lethal temperature jLT& and exposure time of four species af nematodes: open symbols, experiments in winter 19%; f&l. symbols elcperiments in summer 1933 aRd 1974: abbreviations as in Fig. t : Th.c,, ?%~~-isft~s ere-c~.
ECOPHYSIOLOGY
OF SOME MARINE NEMATODES
103
conclusions can be drawn from these experiments. 1) Each of the three species has a distinct survival time curve, the upper lethal temperature at short exposure times being clearly related to the site at which the species occurs in maximum numbers. The species occurring further up the beach, Steinerk~ sterreri, is the most heat-tolerant, whereas TheristusJEoridanus,which is most abundant at the lowest site, is the least tolerant species, with Trefusia schiemeri occupying an intermediate position. The survival curve of Paramon~?~~stera wieseri under anoxic conditions, established in I973 (Wieser et al., 1974) would run slightly beiow that of Theristusfloridanus. 2) No seasonal resistance adaptation can be detected in Steineria sterreri and Trefkia schiemeri, the two species for which comparative summer data are available (Wieser et al., 1974; Wieser, 1975). 3) The Theristus species which dominated the surface layer of the flat in the summer of 1973, T. erectq is much more heat tolerant than T..ftoridanus which replaced it in the winter of 1976 (Fig. 3b). Thus, whereas individual species of nematodes do not seem to be able to adjust their heat tolerance to the thermal demands of the seasons, some species of intertidal habitats may show seasonal fluctuations in population density, with the more heat-tolerant species having their maximum occurrence in summer and the less heat-tolerant ones in winter. Oxygen ronsumptioti
The data for Trefisia schiemeri and Theristus floridanus are given in Fig. 4 and Table 1. The two species differ somewhat in their responses to experimental temperature, as is evident when the Q10 values of acutely determined oxygen consumption are compared. In Trefusia schiemeri the Q10 between 15 ’ and 22 “C is very high (4.45), that between 22 o and 30 “C moderately low (1.58). In TheristusJloridanus the 1.0 T. floridanus
0.8 T 2
g
_ T. schiemeri 0= winter l =summer
0 0
0.6
‘Jl
E
&
0.4
i
0.2-
(,uI Oz mg wet wt- ’ h- I) of two species of nematodes, 7’lzerisrus&viexperimental temperatures: open circles, measurements in in summer 1973: Q 10 values between experimental temperatures of IS Oand 22 “C, and 22 * and 30 “C indicated.
Fig. 4. Oxygen consumption
and Treficsia schiemeri, at three winter 1976; full circles, measurements
danus
Q 10 values of the same two temperature intervals are more or less identical and close to 2.0. Expressed in a different way - oxygen consumption at 15 “C is twice as high in
WOLFGANG
104
Theristus floridanus whereas
WIESER AND FRITZ SCHIEMER
as in Trefusia schiemeri
at the other two experimental
(0.37
temperatures
as against
0.17 ,uI mg-’
both species consume
h-‘),
approxi-
mately the same amount of oxygen. Since it is usually assumed that low QIo values are characteristic of that part of the temperature range which is close to the preferred or optimum temperature range of the two species studied (see Wieser, 1973, for a recent review), one would expect T. schiemeri to be the more thermophilic. This would agree of T. floridanus on the beach in summer
with the absence 1976. Whether
this change
is part of a regular,
long-term
and its presence
in winter
cycle has still to be estab-
lished. TABLE I
Oxygen consumption _ ..__~_..._~~
of two species of nematodes from Tuckers Town Cove Beach, Bermuda, at three experimental temperatures.
_.~------~_.___~-~
--__-.I~~~--_~ O2 consumption
&I mg-’ .zI
_~~ _._
(range)
--
h-‘) +S.D.
~
.-
,-~
_~~~~~ ~
_--~
.-
Wet weight (Fcg) ~
R
(range) .-.
__ ~~--
Q 10 n
~~ l--_
Theristus jloridanus 15 ‘G 22 “C 30 ‘G
0.37 (0.30-0.5 I) 0.50 (0.32-0.62) 0.82 (0.71-0.94)
0.078
0.17 (0.12-0.21) 0.53 (0.39-0.70) 0.67 (0.46-O. 87) 0.46 (0.35-0.60)
0.03
0.11 0.095
5.84 (4.26-7.30) 6.51 (4.92-7.98) 6.46 (4.47-8.15)
1.93
‘I 7) \
2.05
51
Trefusia schienzeri I5 “C
22 ‘C 30 “C winter 1976 30 “C summer 1973
Trefusia schiemeri is clearly
0.11 0.108 0.078
capable
of seasonal
4.19 (3.26-4.87) 2.85 /2.12-3.18) 3.0 (I .85-3.65) 3.55 (3.05-4.95)
acclimatization
61,
4.45
9J 91
I
1.58
12
of its oxygen
consumption. The data of Fig. 4 show that oxygen consumption measured at 30 “C is significantly higher in winter than in summer, and that the latter is about as high as in winter at 22 “C. Since the water temperature in summer is M 30 “C (Wieser, 1975), and in winter
between
16 a and 18 “C, or a little higher when the water on the
flat warms up during low tide, it follows that in T. schiemeri the level of metabolism does not vary much over the range of temperatures encountered by the species in its environment throughout the year. DIXUSSION
Our previous work has emphasized the degree of precision with which the metabolism and the tolerance ranges of some of the meiofauna species of a subtropical low-
ECOPHYSIOLOGY
energy data
beach contribute
resistance
are adjusted
to the micro-environment
a few new aspects
adaptation
implies
on the beach of Tuckers
OF SOME MARINE NEMATODES
Town
in which they live. Our winter
of this phenomenon.
that the distribution
105
First,
the lack of seasonal
of the nematode
Cove is not determined
by habitat
species studied
temperatures
at a
given time of the year but by the maximum temperature to be expected in summer. With this provision in mind, the relation between the horizontal distribution of the dominant nematode species of the beach and their temperature tolerance is as close as could
be expected.
The upper
lethal
temperature
of the dominant
species
of the
highest site, Steineria sterreri, is about 5 “C higher than that of Theristus jloridanus, the major species on the flat, with Trefusia schiemeri occupying an intermediate position both as regards its distribution on the beach and its temperature tolerance. The vertical distribution of the species of Steineria, Theristus, and Paramonhystera (all three genera belonging to the family Monhysteridae) is as distinct as it was in summer, with the two former restricted to the upper 2 cm and the latter to the layers below 2 cm of sediment. In low-energy habitats many species of nematodes seem to be characterized by similarly stable patterns of vertical distribution (Ott & Schiemer, 1973). The factor responsible for the vertical distribution of the oxyphilic species Steineria sterreri, would appear to be a food component, since temperature cannot possibly become limiting for this species and the bar is oxygenated down to a depth of at least 10 cm (Fig. 2). The distribution of Paranzonhystera wieseri depends largely on the existence of reduced conditions in the sediment since normoxic sea water is deleterious to this species (Wieser et al., 1974). The horizontal distribution of TheristusJIoridanus is more variable than that of the other two species. Seasonal migrations may be assumed since so far it has been observed in the upper layers of this beach only in winter, whereas in summer it is a frequent inhabitant of sublittoral habitats (Coull, 1968). If Theristus Jloridanus is indeed a seasonal migrant, this may reflect its low temperature tolerance; it could never survive exposure to the high temperatures on the beach in summer when low tide occurs at noon (Wieser, 1975). The low temperature tolerance of this species finds its counterpart
in the low Q,, between
15 o and 22 “C which is strikingly
than the comparable
value in Trejiisia schiemeri
to high temperatures
(Fig. 3).
lower
(Fig. 4) which is also more resistant
T. schiemeri is the most mobile of the species investigated and this characteristic must depend on its ability to tolerate both normoxic and anoxic conditions (Wieser et al., 1974). Thus, its centre of distribution on the flat is in the anoxic layer below 2 cm of sediment but on the shoulder it is in the oxygenated upper 2 cm (Fig. 2). Apart from its tolerance of anoxic conditions the species is much less heat tolerant than Steineria sterreri and is particularly sensitive to alkaline pH. This caused us to speculate previously (Wieser et al., 1974; Wieser, 1975) that in summer Trefusia schiemeri only migrates to the surface of the sediment on relatively cool days. In winter neither high temperature nor high pH values are likely to become limiting factors on the beach and this may be the reason why at this time of year T. schiemeri is able to
106
WOLFGANG
WIESER
AND
FRITZ
SCHIEMER
occupy the upper layer of the sediment in vast numbers. On the ffat the species is less abundant than on the shoulder and more or less limited to the anoxic layers below 2 cm. This may be the result of competition with other species including Theristus Jloridanus which have to stay in the upper oxygenated layers of the sediment since they are incapable of toIerating anoxic conditions for more than a short time. In conclusion it may be said that on a subtropical low-energy beach the spatial and temporal patterns of distribution of four species of nematodes are strongly correlated with temperature, p&I, Eh, P,,, and water content of the sediment, and equahy clearly reflect certain physiological characteristics of the animals, such as temperature tolerance and temperature relation of oxygen consumption. This is taken as further proof that in this type of habitat the metabolic capacities of many meiofauna species are closely adjusted to the micro-environment in which they live. ACKNOWLEDGEMENTS
This investigation was supported by a special grant from the Ministry of Education of Austria and by Project No. 1852 of the Fonds zur Fiirderung der wissenschaftlichen Forschung of Austria. We are grateful to Dr. W. Sterrer and the staff at the Bermuda Biological Station who have been most helpful throughout our work.
REFERENCES COULL,B. C., 1968. Shallow water meiobenthos of the. Bermuda platform. Thesis, Lehigh University, 132 pp. FARRIS, R. A., 1976. Systematics and ecology of Gnathostomulida from North CarolinaandBermuda. Thesis, University of North Carolina, Chapel Hill, N.C., 188 pp. KLEKoWSKi, R. Z., 1971. Cartesian diver microsp~rom~try for aquatic animals. Pal. Arch. H~drobjul., Vol. 18, pp, 93-114. OTT, .I. A., in press. New freeliving marine nematodes from the west Atlantic. I. Four new species from Bermuda with a discussion of the genera C~ytolaimiunzand Rhabdocorna Cobb 1920. Zool. An,-. OTT, J. A. & F. SCXIEMER,1973. Respiration and anaerobiosis of free living nematodes from marine and iimnic sediments. Neth. J. Sea Res., Vol. 7, pp. 233-243. PRECHT,H., 1955. Wechselwarme Tiere und Pflanzen. In, Temperatur und Leben, edited by H. Precht, J. Christophersen & H. Hens-l, Springer Verlag, Berlin, S. l-177. PRECHT, H., 1958. Concepts of the temperature adaptation of unchanging reaction systems of coldblooded animals. ln, Ph~~~ofugicu~oduptution, edited by C. L. Presser, Am. Physiol. Sot., Wasttington D.C., pp. 50-78. WIESER,W., 1973. Temperature relations of ectotherms. A speculative review. In, Effects oftenzperature on ectothermic organisms, edited by W. Wieser, Springer Verlag, Berlin, pp. l-23. WIESER,W., 1975. The m~iofauna as a tool in the study of habitat heterogeneity. Ecophysiolog~cal aspects. A review. Cak. Biol. mar., T. 16, pp. 647-670. WIESER,W. & B. HOPPER, 1967. Marine nematodes of the east coast of North America. I. Florida. Bull. Mus. camp. Zool. Hatv., Vol. 135, pp. 239-344. WIESER,W., J. OTT, F. SCHIEMEJ~& E. GNAIGER, 1974. An ecophysiological study of some meiofauna species inhabiting a sandy beach at Bermuda. Mar. Biol., Vol. 26, pp. 235-248. WIESER, W. & M. ZECH, 1976. Dehydrogenases as a tool in the study of marine sediments. Mar. Biol., Vol. 36, pp. 113-122.
Biol. Ecol.,
Q Elsevier/North-Holland
1977, Vol. 26, pp. 97-106;
Biomedical Press
THE ECOPHYSIOLOGY
OF SOME MARINE NEMATODES
BERMUDA:
SEASONAL
FROM
ASPECTS
WOLFGANG WIESER Institut fiir Zoophysiologie
der Unioersitiit,
Innsbruck,
osterreich
and FRITZ SCHIEMER Lehrkanzel
fiir Limnologie
der Uniuersitiit,
Wien, i)sterreich
Abstract: In the winter of 1976 the horizontal and vertical distribution, temperature tolerance, and oxygen consumption at three experimental temperatures were determined for several species of nematodes inhabiting a low-energy beach in Bermuda. The results are compared with those of previous summer investigations carried out on the same beach. The three most abundant species of nematodes on the beach, Steineria sterreri Ott, Trefitsia schiemeri Ott and Theristllsfloridunus Wieser & Hopper show distinct patterns of distribution as well as distinct survival-time curves when upper lethal temperature is plotted against exposure time. No seasonal resistance adaptation to high temperature occurs in Steineriu sterreri and Trefusia schiemeri, the two species for which comparative summer data are available. Theristus erectas, which dominated the flat in summer, is much more heat tolerant than T.Jloridanus which replaced it in winter. Oxygen consumption at 15 “C is twice as high in T. ,jforidanus as in Trejiisiu schiemeri, whereas at 22 ’ and 30 “C both species consume approximately the same amount of oxygen. T. schiemeri is capable of seasonal adaptation of Qo, inasmuch as it consumes just about as much oxygen in winter at 22 “C as in summer at 30 “C. The seasonal data support the suggestion that on a subtropical low-energy beach the metabolic capacities of many meiofauna species are closely adjusted to the micro-environment in which they live.
An earlier investigation
into the ecophysiology
of the meiofauna
inhabiting
a sub-
tropical beach in Bermuda (Wieser et al., 1974; Wieser, 1975) led to the conclusion that the upper lethal temperatures and pH values of most of the species studied are closely related to their vertical distribution
in the sediment
as well as to the maximum
values of temperature and pH measured at the centre of distribution of each species, and that there is a relation between the respiratory rates of nematodes and their vertical distribution in the sediment. Furthermore, the acclimation of nematodes to different environmental temperatures has no effect on their oxygen consumption measured at 30 “C. It is of interest to determine whether season has any effect on these relations which were established during the summer. For example, if it were generally 1 Contribution
No. 683 from the Bermuda Biological Station for Research. 97
WOLFGANG
98
WIESER AND FRITZ SCHIEMER
true that the upper lethal temperatures &he maximum
temperatures
lower vaIues of LT,, “resistance adaptation”
of marine
experienced
in winter
than
meiofauna
in their habitats, in summer,
species are very close to one would
i.e., a considerable
expect much amount
in the sense of Precht (1955, 1958). In order to consider
and some related problems
an investigation
of selected nematode
Town Cove Beach was carried out in February MATERIAL AND
of this
species from Tuckers
1976.
METHODS
AREA OF THE INVESTIGATION
Field measurements and sampling were carried out at Tuckers Town Cove Beach, Bermuda. The locality has been described briefly by Wieser ef al. (1974) and by Wieser & Zech (1976). A thorough analysis of the IocaIity has more recently been completed by Farris (1976) and it is simplest to quote the following facts which are pertinent to our study. “Tuckers Town Cove Beach is Iocated in Tucker’s Town Bay on the SW side of Castle Harbour . . ,. A perpendicular bar extends across the beach 62 m from spring high tide Ievel (S.H.T.L.). The bar restricts water movement along the landward side of the beach at low tide. Mean slope of the beach to the bar is approximately 1.5 % with the greatest decline occurring in the first 13 m from S.H.T.L. Seaward from the bar, the beach slopes on an average of 4 % descending subiittorally into a deep channel. Tidal ranges seldom exceed I m vertically and 85 m horizontally. Sand is calcareouswith a mean grain size of 250 pm (4 2) . . . Stands of red mangroves (Rhizophora mangle) lie adjacent to the beach on the northwest side and contribute heavily to organic matter in the beach ecosystem. The reducing nature of TTCB is particularly evident during low tide at which time the odor of hydrogen sulfide can be detected.” sediments
Perhaps it should be pointed out that for a marine ecoIogist used to silicate in temperate regions, this beach is unusual insofar as it consists of medium-
sized, well sorted sand of the type one would expect on a high-energy
beach, whereas
its rich content
only a few mm
of organic
below the surface indicate
matter
as well as a reducing
a low-energy
environment
beach.
SAMPLES
Samples were taken at Iow tide at three sites along an east-west transect across the intertidal beach, above and below mean water leve1 (Fig. 1). Cores with a cross section of 10 cm2 were taken and sectioned to give the following vertical zones: O-l, 1-2, 2-5, 5-10 cm. For the experiments animals were separated from bulk samples by the usual shaking and decanting procedure. The water content of aliquot sediment samples from the top 1 cm layer was determined by weighing and drying at 100 “C. Redox potentials were measured with a Corning portable voltmeter using a platinum electrode and a Corning calomel reference electrode. Temperature was measured with a mercury thermometer.
ECOPHYSIOLOGY
OF SOME
MARINE
NEMATODES
99
SPECIES
The following species of nematodes were studied: Trefusia schiemeri Ott (in press) 1 Tripyloides n.sp. in Wieser et al. (1974) and Wieser (1975); Theristars Jloridanus Wieser & Hopper (1967); ~~~~~e~~a sterreri Ott (in press) = Steineri n.sp. in Wieser (1975); and Paramonhystera wieseri Ott (in press) = Paramonhystera n.sp. in Wieser et al. (1974) and Wieser (1975). SURVIVAL
EXPERIMENTS
In order to establish upper lethal temperatures groups of animals (mostly 20 to 30, sometimes only 10) were put into filtered, normoxic sea water in small vials. The stoppered vials were submerged in a water bath and subjected to high temperatures for 1 to 10 h. Results are expressed as LTSO, determined from the regression lines of temperature on survival (see Wieser et al., 1974). OXYGEN CONSUMPTION
Adult males of two of the species studied were separated (shaking and decantingtechnique) from large samples of sand usually taken within 24 h before the experiments. Before sorting, the samples were stored in the laboratory at x 20 “C. The experimental animals were held in filtered sea water, containing 1000 I.U. of streptomycin and 1000 I.U. of penicillin per ml at the experimental temperature for 1 h. The oxygen consumptions of individual animals was measured using ‘stoppered Cartesian divers’ (0.5-1.5 ~1) as described in detail by Klekowski (197l),at 15 O,22 ‘, and 30 “C. The divers were filled with sea water filtered through a 0.45 pm Millipore filter and re-aerated. The animals were positioned in the divers by means of capillary pipettes. After loading, the divers were put into the flotationvessels and the equilibrium pressure was roughly adjusted. Manometric reading started 1 h later and lasted 3-6 h. Experiments giving readings which were not linear with time were discarded. Control runs were carried out at each experimental temperature in order to check the thermostability of the water-bath and to establish the equilibrium time required for each experimental temperature. Camera-lucida drawings were used to calculate the volumes of the experimental animals. Weight-specific respiratory rates in ~1 O2 mg-” h-’ are based on these volume determinations, assuming a specific gravity of 1.00.
RESULTS TEMPERATURE
According to the records kept at the Bermuda Biological Station the following ranges of temperature (“C) prevailed in the months December, 1975 to February,
WOLFGANG
100
1976 (the water temperature Reach and the air temperature
WIESER AND FRITZ SCHIEMER
was measured off the dock of the Biostation at Ferry at the dock, both in the morning).
December Maximum “C Minimum “C
Water 20.8 17.2
January
February
Air
Water
Air
Water
Air
21.6 16.1
18.6 16.1
21.1 14.4
18.8 16.4
22.1 13.1
At Tuckers Town Cove Beach at low tide the water remaining on the flat and in tidal pools might warm up several degrees above the temperature of the offshore water. During the period of our work (4th-25th Feb.) we recorded maximum water temperatures on the flat of 26 “C, maximum surface temperatures of exposed sand of 24.5 “C: values as high as these occurred, however, only on a few days at noon. Usually, the temperature of the sand surface at low tide varied between 16 ’ and 23 “C. Minimum values measured on the sand surface were 12.5 * to 13 “C. REDOX POTENTfALS
Several series of Eh measurements were carried out at the three sites. The ranges of Eh values recorded, from the surface to 10 cm depth, are given in Fig. 2. The bar sand remains oxygenated down to the greatest depth measured, whereas on the flat the sediment is highly reduced below 1 cm. The shoulder site occupies an intermediate position with the redox discontinuity layer situated between I and 2 cm. These differences in the degree of reduction of the sediment between the three sites are closely correlated with their elevation above low-tide level and with the water content of the sand (Fig. I). The higher the site above the low tide level, the more unsaturated is the top layer and the more oxygenated are the lower layers of the sediment core. DISTRIBUTION
OF NEMATODES
Samples were taken at three sites on the beach, namely ‘bar’, ‘shoulder’ and ‘flat’. The position of these along an east-west transect of the beach, the water content of the top layer of sediment at low tide, as well as the abundance (per 10 cm3 wet sediment) of the three dominant species of nematodes found at these sites are summarized in Fig. 1. The ‘bar’ site is clearly dominated by Stein&a sterreri, with very few other species of nematodes present. The ‘shoulder’ site is characterized by the dominance of Trefusiu schiemeri: many other species of nematodes are present but none in comparable numbers. The surface tayer of this site also has abundant harpacticoids, probably belonging to the species studied in 1973, i.e., Roberfsonia lcnoxi (Thompson & A. Scott), Amphia~co~de~ ~~bdebii~~ (Willey) and Ps~~~ocarnp~s nsp. (see Wieser et al., 1974). The ‘flat’ site is richest in nematode species and the dominance of Ther~~t~s~oridon~~ is not as striking as that of Steineria sterreri and Trefusia s~t~~e~~eri
ECOPHYSIOLOGY
at the other two sites. The anaerobic occurs in moderate
numbers
East
OF SOME
MARINE
species Paramonhystera wieseri, studied in 1973,
below 2 cm both at the shoulder
bar
HWL
0
101
NEMATODES
shoulder @
and at the flat site. West ,m 1.0
________---------
p 40 m
0.8 i% 0.6 ” z 0.4 m
20 aI” 30 0, 10
0.2
Fig. 1. An east-wast profile of Tuckers Town Cove Beach, Bermuda, showing thz three sampling sites: bar (I), shoulder (2), and flat (3): upper graph shows water content (g water/g wet sediment weight x 100) of the uppx cm of sand at four points along the transect: lower graph gives the abundance (individuals/lo cm3 sediment) of three dominant species of nematodes at the three sampling sites: Sst., Steineria sterreri; T.s., Trefuria schiemzri: Th.f., Theristus fioridanus; HWL, mean high water level; LWL, mean low water level.
Steineria, Trefusia, and Paramonhystera have been found
at this beach regularly
since the summer of 1973 when our research started. Theristusjoridanus, however, is a newcomer to this locality. Although one of the most frequent inhabitants of shallowwater sediments in the area, particularly in Caste1 Harbor at 3 m depth (Coull, 1968), it had not been found previously on Tuckers Town Cove Beach. In 1973, the upper sediment layers of the flat were dominated by T. erectus (Wieser & Hopper, 1967). In the summers of 1974 and 1975, Theristus sp. seemed to have become scarce but no detailed analysis of its distribution was made at those times. In February 1976, T. erectus had definitely
disappeared
and T. floridanus made its appearance.
Vertical distribution The vertical distribution of the three nematode species dominating the three sites, as well as that of Paramonhystera wieseri, is summarized in Fig. 2. The vertical and horizontal patterns of distribution are distinct and may serve to characterize the three sites studied. Trefusia schiemeri, so abundant in the upper 2 cm of the shoulder site, does not occupy this zone to any noteworthy degree on the flat, but finds its centre of abundance there below a depth of 2 cm. This maybe the result of competition with Theristus joridanus which appears to be the more successful surface species in the flat, the less successful one on the shoulder. The distribution of Paramonhystera wieseri is clearly correlated with the occurrence of reducing conditions in the sediment.
WOLFGANG
102
WESER
AND FRITZ SCHIEMER
i
o-21-
-__i-Le.t
13
5
7
9 haursexposura
7
9
Fig, 3. Upper lethal temperature jLT& and exposure time of four species af nematodes: open symbols, experiments in winter 19%; f&l. symbols elcperiments in summer 1933 aRd 1974: abbreviations as in Fig. t : Th.c,, ?%~~-isft~s ere-c~.
ECOPHYSIOLOGY
OF SOME MARINE NEMATODES
103
conclusions can be drawn from these experiments. 1) Each of the three species has a distinct survival time curve, the upper lethal temperature at short exposure times being clearly related to the site at which the species occurs in maximum numbers. The species occurring further up the beach, Steinerk~ sterreri, is the most heat-tolerant, whereas TheristusJEoridanus,which is most abundant at the lowest site, is the least tolerant species, with Trefusia schiemeri occupying an intermediate position. The survival curve of Paramon~?~~stera wieseri under anoxic conditions, established in I973 (Wieser et al., 1974) would run slightly beiow that of Theristusfloridanus. 2) No seasonal resistance adaptation can be detected in Steineria sterreri and Trefkia schiemeri, the two species for which comparative summer data are available (Wieser et al., 1974; Wieser, 1975). 3) The Theristus species which dominated the surface layer of the flat in the summer of 1973, T. erectq is much more heat tolerant than T..ftoridanus which replaced it in the winter of 1976 (Fig. 3b). Thus, whereas individual species of nematodes do not seem to be able to adjust their heat tolerance to the thermal demands of the seasons, some species of intertidal habitats may show seasonal fluctuations in population density, with the more heat-tolerant species having their maximum occurrence in summer and the less heat-tolerant ones in winter. Oxygen ronsumptioti
The data for Trefisia schiemeri and Theristus floridanus are given in Fig. 4 and Table 1. The two species differ somewhat in their responses to experimental temperature, as is evident when the Q10 values of acutely determined oxygen consumption are compared. In Trefusia schiemeri the Q10 between 15 ’ and 22 “C is very high (4.45), that between 22 o and 30 “C moderately low (1.58). In TheristusJloridanus the 1.0 T. floridanus
0.8 T 2
g
_ T. schiemeri 0= winter l =summer
0 0
0.6
‘Jl
E
&
0.4
i
0.2-
(,uI Oz mg wet wt- ’ h- I) of two species of nematodes, 7’lzerisrus&viexperimental temperatures: open circles, measurements in in summer 1973: Q 10 values between experimental temperatures of IS Oand 22 “C, and 22 * and 30 “C indicated.
Fig. 4. Oxygen consumption
and Treficsia schiemeri, at three winter 1976; full circles, measurements
danus
Q 10 values of the same two temperature intervals are more or less identical and close to 2.0. Expressed in a different way - oxygen consumption at 15 “C is twice as high in
WOLFGANG
104
Theristus floridanus whereas
WIESER AND FRITZ SCHIEMER
as in Trefusia schiemeri
at the other two experimental
(0.37
temperatures
as against
0.17 ,uI mg-’
both species consume
h-‘),
approxi-
mately the same amount of oxygen. Since it is usually assumed that low QIo values are characteristic of that part of the temperature range which is close to the preferred or optimum temperature range of the two species studied (see Wieser, 1973, for a recent review), one would expect T. schiemeri to be the more thermophilic. This would agree of T. floridanus on the beach in summer
with the absence 1976. Whether
this change
is part of a regular,
long-term
and its presence
in winter
cycle has still to be estab-
lished. TABLE I
Oxygen consumption _ ..__~_..._~~
of two species of nematodes from Tuckers Town Cove Beach, Bermuda, at three experimental temperatures.
_.~------~_.___~-~
--__-.I~~~--_~ O2 consumption
&I mg-’ .zI
_~~ _._
(range)
--
h-‘) +S.D.
~
.-
,-~
_~~~~~ ~
_--~
.-
Wet weight (Fcg) ~
R
(range) .-.
__ ~~--
Q 10 n
~~ l--_
Theristus jloridanus 15 ‘G 22 “C 30 ‘G
0.37 (0.30-0.5 I) 0.50 (0.32-0.62) 0.82 (0.71-0.94)
0.078
0.17 (0.12-0.21) 0.53 (0.39-0.70) 0.67 (0.46-O. 87) 0.46 (0.35-0.60)
0.03
0.11 0.095
5.84 (4.26-7.30) 6.51 (4.92-7.98) 6.46 (4.47-8.15)
1.93
‘I 7) \
2.05
51
Trefusia schienzeri I5 “C
22 ‘C 30 “C winter 1976 30 “C summer 1973
Trefusia schiemeri is clearly
0.11 0.108 0.078
capable
of seasonal
4.19 (3.26-4.87) 2.85 /2.12-3.18) 3.0 (I .85-3.65) 3.55 (3.05-4.95)
acclimatization
61,
4.45
9J 91
I
1.58
12
of its oxygen
consumption. The data of Fig. 4 show that oxygen consumption measured at 30 “C is significantly higher in winter than in summer, and that the latter is about as high as in winter at 22 “C. Since the water temperature in summer is M 30 “C (Wieser, 1975), and in winter
between
16 a and 18 “C, or a little higher when the water on the
flat warms up during low tide, it follows that in T. schiemeri the level of metabolism does not vary much over the range of temperatures encountered by the species in its environment throughout the year. DIXUSSION
Our previous work has emphasized the degree of precision with which the metabolism and the tolerance ranges of some of the meiofauna species of a subtropical low-
ECOPHYSIOLOGY
energy data
beach contribute
resistance
are adjusted
to the micro-environment
a few new aspects
adaptation
implies
on the beach of Tuckers
OF SOME MARINE NEMATODES
Town
in which they live. Our winter
of this phenomenon.
that the distribution
105
First,
the lack of seasonal
of the nematode
Cove is not determined
by habitat
species studied
temperatures
at a
given time of the year but by the maximum temperature to be expected in summer. With this provision in mind, the relation between the horizontal distribution of the dominant nematode species of the beach and their temperature tolerance is as close as could
be expected.
The upper
lethal
temperature
of the dominant
species
of the
highest site, Steineria sterreri, is about 5 “C higher than that of Theristus jloridanus, the major species on the flat, with Trefusia schiemeri occupying an intermediate position both as regards its distribution on the beach and its temperature tolerance. The vertical distribution of the species of Steineria, Theristus, and Paramonhystera (all three genera belonging to the family Monhysteridae) is as distinct as it was in summer, with the two former restricted to the upper 2 cm and the latter to the layers below 2 cm of sediment. In low-energy habitats many species of nematodes seem to be characterized by similarly stable patterns of vertical distribution (Ott & Schiemer, 1973). The factor responsible for the vertical distribution of the oxyphilic species Steineria sterreri, would appear to be a food component, since temperature cannot possibly become limiting for this species and the bar is oxygenated down to a depth of at least 10 cm (Fig. 2). The distribution of Paranzonhystera wieseri depends largely on the existence of reduced conditions in the sediment since normoxic sea water is deleterious to this species (Wieser et al., 1974). The horizontal distribution of TheristusJIoridanus is more variable than that of the other two species. Seasonal migrations may be assumed since so far it has been observed in the upper layers of this beach only in winter, whereas in summer it is a frequent inhabitant of sublittoral habitats (Coull, 1968). If Theristus Jloridanus is indeed a seasonal migrant, this may reflect its low temperature tolerance; it could never survive exposure to the high temperatures on the beach in summer when low tide occurs at noon (Wieser, 1975). The low temperature tolerance of this species finds its counterpart
in the low Q,, between
15 o and 22 “C which is strikingly
than the comparable
value in Trejiisia schiemeri
to high temperatures
(Fig. 3).
lower
(Fig. 4) which is also more resistant
T. schiemeri is the most mobile of the species investigated and this characteristic must depend on its ability to tolerate both normoxic and anoxic conditions (Wieser et al., 1974). Thus, its centre of distribution on the flat is in the anoxic layer below 2 cm of sediment but on the shoulder it is in the oxygenated upper 2 cm (Fig. 2). Apart from its tolerance of anoxic conditions the species is much less heat tolerant than Steineria sterreri and is particularly sensitive to alkaline pH. This caused us to speculate previously (Wieser et al., 1974; Wieser, 1975) that in summer Trefusia schiemeri only migrates to the surface of the sediment on relatively cool days. In winter neither high temperature nor high pH values are likely to become limiting factors on the beach and this may be the reason why at this time of year T. schiemeri is able to
106
WOLFGANG
WIESER
AND
FRITZ
SCHIEMER
occupy the upper layer of the sediment in vast numbers. On the ffat the species is less abundant than on the shoulder and more or less limited to the anoxic layers below 2 cm. This may be the result of competition with other species including Theristus Jloridanus which have to stay in the upper oxygenated layers of the sediment since they are incapable of toIerating anoxic conditions for more than a short time. In conclusion it may be said that on a subtropical low-energy beach the spatial and temporal patterns of distribution of four species of nematodes are strongly correlated with temperature, p&I, Eh, P,,, and water content of the sediment, and equahy clearly reflect certain physiological characteristics of the animals, such as temperature tolerance and temperature relation of oxygen consumption. This is taken as further proof that in this type of habitat the metabolic capacities of many meiofauna species are closely adjusted to the micro-environment in which they live. ACKNOWLEDGEMENTS
This investigation was supported by a special grant from the Ministry of Education of Austria and by Project No. 1852 of the Fonds zur Fiirderung der wissenschaftlichen Forschung of Austria. We are grateful to Dr. W. Sterrer and the staff at the Bermuda Biological Station who have been most helpful throughout our work.
REFERENCES COULL,B. C., 1968. Shallow water meiobenthos of the. Bermuda platform. Thesis, Lehigh University, 132 pp. FARRIS, R. A., 1976. Systematics and ecology of Gnathostomulida from North CarolinaandBermuda. Thesis, University of North Carolina, Chapel Hill, N.C., 188 pp. KLEKoWSKi, R. Z., 1971. Cartesian diver microsp~rom~try for aquatic animals. Pal. Arch. H~drobjul., Vol. 18, pp, 93-114. OTT, .I. A., in press. New freeliving marine nematodes from the west Atlantic. I. Four new species from Bermuda with a discussion of the genera C~ytolaimiunzand Rhabdocorna Cobb 1920. Zool. An,-. OTT, J. A. & F. SCXIEMER,1973. Respiration and anaerobiosis of free living nematodes from marine and iimnic sediments. Neth. J. Sea Res., Vol. 7, pp. 233-243. PRECHT,H., 1955. Wechselwarme Tiere und Pflanzen. In, Temperatur und Leben, edited by H. Precht, J. Christophersen & H. Hens-l, Springer Verlag, Berlin, S. l-177. PRECHT, H., 1958. Concepts of the temperature adaptation of unchanging reaction systems of coldblooded animals. ln, Ph~~~ofugicu~oduptution, edited by C. L. Presser, Am. Physiol. Sot., Wasttington D.C., pp. 50-78. WIESER,W., 1973. Temperature relations of ectotherms. A speculative review. In, Effects oftenzperature on ectothermic organisms, edited by W. Wieser, Springer Verlag, Berlin, pp. l-23. WIESER,W., 1975. The m~iofauna as a tool in the study of habitat heterogeneity. Ecophysiolog~cal aspects. A review. Cak. Biol. mar., T. 16, pp. 647-670. WIESER,W. & B. HOPPER, 1967. Marine nematodes of the east coast of North America. I. Florida. Bull. Mus. camp. Zool. Hatv., Vol. 135, pp. 239-344. WIESER,W., J. OTT, F. SCHIEMEJ~& E. GNAIGER, 1974. An ecophysiological study of some meiofauna species inhabiting a sandy beach at Bermuda. Mar. Biol., Vol. 26, pp. 235-248. WIESER, W. & M. ZECH, 1976. Dehydrogenases as a tool in the study of marine sediments. Mar. Biol., Vol. 36, pp. 113-122.