REVIEWS
Seasonality in coastal benthic
ecosystems
Rafel Coma, Marta Ribes, Josep-Maria Gili and
Mikel Zabala
L
ranging from abundance to complete energy budget studies and
production of chemical defenses.
They provide evidence that the
seasonal pattern of benthic
suspension feeders, observed in
cold temperate seas, might not be
generally applicable to warm
temperate seas such as the
Mediterranean.
In the Mediterranean, most
benthic hydrozoan species exhibit
a seasonal pattern, with reproduction in spring or autumn and
growth from autumn to spring.
Most hydrozoans disappear during the summer, leaving only dormant basal stolons5,6 (Fig. 2).
These observations contrast with
the pattern observed in cold temperate seas, where dormant basal
stolons occur during winter7 and
activity occurs in the summer
months3,7. Although winter dormancy (hibernation) is normal in
Seasonal patterns in benthic
cold temperate areas, summer
Rafel Coma, Marta Ribes and Josep-Maria Gili are at
suspension feeders
dormancy (aestivation) might ocFor historical reasons (the early the Institut de Ciències del Mar (CSIC), Passeig Joan cur in warmer seas3. However,
de Borbó s/n, 08039 Barcelona, Spain
development of marine biology
most of these studies refer only to
([email protected]; [email protected];
occurred in coastal temperate [email protected]); Mikel Zabala and Rafel Coma are at seasonal variations in abundance
areas), studies on seasonal patand do not distinguish the timing
the Dept of Ecology at the Faculty of Biology,
terns of benthic suspension feedof the productive processes.
University of Barcelona, Diagonal 645, 08028
ers have been conducted primarStudies of several MediterBarcelona, Spain ([email protected]).
ily in cold temperate seas3. From
ranean colonial ascidians8,9, three
these studies, an annual pattern
bivalve species10,11 and four speof benthic suspension feeder
cies of anthozoans12,13, all show
dynamics has emerged. This patthat reproductive output and
tern is characterized by an increase in activity and in sec- growth rate are highest during winter (or over both the winondary production of most taxa during spring and summer ter and spring). During the summer, activity in these taxa
(Fig. 1). Activity and secondary production decrease in decreases (several species of colonial ascidians become
autumn; these factors reach a minimum in winter, when dormant)8,9, anthozoans exhibit a marked decrease in all
some species undergo winter dormancy or hibernation activities12,13 and shell growth in the bivalves ceases
(Fig. 1). The most characteristic aspects of this seasonal altogether10,11 – a pattern in marked contrast to that
pattern are winter dormancy and summer activity of described for bivalves in cold temperate seas10.
organisms. Usually, temperature is suggested as the main
There is growing evidence that seasonal patterns of
cause for winter dormancy, owing to its direct effect on the activity and secondary production of benthic suspension
rate of chemical reactions and its indirect effect on other feeders in warm temperate seas, such as the Mediterphysical parameters of the environment4.
ranean, are characterized by aestivation (Fig. 2). This contrasts with the seasonal pattern observed in cold temperSeasonality in Mediterranean benthic suspension
ate seas, where hibernation and summer activity are the
feeders
common features3 (Fig. 1). Nevertheless, aestivation
Recently, the number of studies of benthic suspension processes differ among taxa (Box 1).
feeders in the Mediterranean has increased using species
from different taxa (cnidarians, bivalve molluscs, ascidians How general is summer dormancy?
and sponges). These studies refer to different aspects of the Studies of sponges and solitary ascidians suggest patseasonal variation of benthic suspension feeder dynamics, terns of dynamics that differ from cnidarians, bivalve
ittoral ecosystems are subject to great environmental
variability; therefore, life
cycles of marine organisms show
marked seasonal patterns in
growth, reproduction and abundance. This is especially evident
in cold temperate seas1,2, but also
occurs in tropical areas. Benthic
suspension feeders are sessile
poikilotherms and are thus
strongly influenced by physical
factors in their local environment.
This heterogeneous and widespread group of organisms is a
convenient group in which to
search for patterns of responses
to environmental factors. The dependence of benthic suspension
feeders on the spatio-temporal
variability of water column resources makes them a useful system to understand physical and
biological coupling in the ocean.
448
For historical reasons, knowledge about
seasonality in the dynamics of marine
benthic suspension feeders from
temperate areas comes mainly from
studies of cold temperate seas. Recent
surveys of Mediterranean taxa show
different patterns from those observed in
cold temperate seas, which are
characterized by winter dormancy. In the
Mediterranean, summer dormancy
predominates among taxa and appears to
be related to energetic constraints.
Temperature and food availability are
crucial to the dynamics of benthic
suspension feeders. However, because
these factors tend to be positively
correlated in cold temperate seas, it is
difficult to distinguish between their
effects. Such correlation does not occur in
Mediterranean ecosystems. The contrast
between recent studies in the
Mediterranean and in other areas can help
to disentangle confounded environmental
controls.
0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(00)01970-4
TREE vol. 15, no. 11 November 2000
REVIEWS
molluscs and colonial ascidians. Reproductive investCold temperate – hibernation
ment in several species of
Mediterranean sponge is
Bryozoa
Flustra foliacea
highest between spring and
Bugula flabellata
summer, the time when
spawning occurs14,15 (Fig. 3).
Chartella papyracea
Asexual reproduction occurs
Bivalvia
Cerastoderma edule
during autumn and winter,
and does not overlap with
Porifera
Halichondria panicea
the period of sexual repro14
duction . Seasonal variation
Hydrozoa
Tubularia indivisa
in growth rate has been
Tubularia crocea
examined in only one
species of sponge (Crambe
Tubularia larynx
crambe), where highest
Plumularia cetacea
growth occurs during summer and autumn. This
Ascidiacea
Perophora sagamiensis
species also exhibits a
marked seasonal pattern in
Perophora formosona
the production of chemical
Ciona intestinalis
defenses, with the highest
concentration occurring in
J
F
M
A
M
J
J
A
S
O
N
D
late autumn16. However,
Winter
Spring
Summer
Autumn
paradoxically, a resting or
dormant stage has been
Dormancy/hibernation
Growth
Sexual reproduction
observed in between 5% and
20% of the population of this
Trends in Ecology & Evolution
species in late summer and
Fig. 1. Examples of suspension feeders, from different benthic taxa, in cold temperate seas showing the annual
autumn17. In contrast to
activity patterns (i.e. secondary production and activity) that are characterized by hibernation (winter dormancy).
colonial species, solitary
Compiled from Refs 5,7,8,34,35.
ascidians invest most in
reproduction during the
summer18 and growth is also
highest at this time19 (Fig. 3).
complex evolutionary history of the sea, and to the presAlthough studies of benthic suspension feeders in the ent range of climatic and hydrologic conditions found in
Mediterranean show that aestivation is the normal phe- the Mediterranean, which allows species from different
nomenon, studies on sponges and solitary ascidians indi- biogeographic categories to coexist there.
Seasonal patterns of sponges and solitary ascidians do
cate that exceptions can be found. Furthermore, hibernation also occurs in the Mediterranean (Fig. 2). Instances not differ from those of the other species and taxa in cold
of hibernation come from two main sources: (1) studies in temperate seas (Fig. 1), but they do in the Mediterranean
localities where climatic and hydrological conditions differ (Fig. 3). Because their seasonal patterns are strongly
from the general pattern, and (2) studies of species with related to dominant environmental factors, this discreptropical biogeographic affinities. Actual instances of these ancy could provide a focus for research into the causes of
two sources of hibernation are the colonial ascidian the two types of pattern observed in Mediterranean
Botrylloides leachi and the hydrozoan Halocordyle disticha. benthic suspension feeders.
In winter, colonies of B. leachi lack functional filtering
zooids and undergo a succession of changes that culmi- Major ecological factors affecting benthic
nate in a condition of winter quiescence. This process has suspension feeders
been observed at the Venetian lagoon (NW Adriatic Sea) Activity patterns of most hydrozoan species correspond to
and can be attributed to the fact that temperature values in annual cycles of temperature20. However, temperature is
winter (usually ,108C, but during certain periods ,58C) not the sole factor responsible for their seasonal cycles7;
are much lower than the values in the general Mediter- indeed, in the Mediterranean, temperature plays a direct
ranean pattern (128C). The hydrozoan H. disticha is com- minor role in determining the disappearance of hydromon in tropical regions of the Atlantic, Pacific and Indian zoan populations6. Two main hypotheses have been put
Oceans. In the Mediterranean, this species is typically pres- forward to explain the decline of hydrozoan populations:
ent in summer but remains dormant in winter. The same space competition with algae and energy shortage. To
hibernation behaviour has been observed in cold temper- date, results suggest that both hypotheses might be
ate seas, which has been attributed to the tropical affin- involved, although working at different periods. Most
ities of the hydrozoan. The species can survive tempera- hydrozoan populations decrease abundance in spring, a
tures as low as 38C while dormant20. The complexity of the period when prey availability is high but coincides with an
Mediterranean Sea is indicated by the presence of both increase in algal abundance. In shallow waters, algal comaestivation and hibernation processes. This complexity is, munities strongly affect the structure of the benthos in
in part, attributable to its high biodiversity – the Mediter- spring (Box 2). Algae might outcompete a considerable
ranean represents only 0.8% of the surface area of the number of hydrozoan species7. Therefore, competition for
oceans but contains 6.3% of the world’s marine species21. substratum appears to be related to the decrease in abunThis high biodiversity level has been attributed to the dance of hydrozoan populations in spring, albeit the role of
TREE vol. 15, no. 11 November 2000
449
REVIEWS
Warm temperate – aestivation
Ascidiacea
Aplidium aff. conicum
Pseudodistoma crucigaster
Polysyncraton lacazei
Botrylloides leachi
1 of 19 species
18 of 19 species
Most of 36 colonial species
Bivalvia
Venus verrucosa
Donax trunculus
Chamalea gallina
Anthozoa
Parazoanthus axinellae
Alcyonium acaule
Eunicella cavolini
Paramuricea clavata
Hydrozoa
7 species
35 species
4 of 29 species
25 of 29 species
Most of 73 species
Eudendrium glomeratum
J
F
M
Winter
Dormancy
Growth
Feeding activity
Abundance
A
M
Spring
J
J
A
Summer
S
O
N
D
Autumn
Sexual reproduction
Trends in Ecology & Evolution
Fig. 2. Data on the annual activity patterns (i.e. secondary production and activity) of benthic suspension feeders
from different taxa exhibiting aestivation (summer dormancy) in the warm temperate Mediterranean. Compiled
from Refs 5,6,8,10–13.
Box 1. Aestivation processes
Cycles of activity and dormancy are common among benthic invertebrates. In the Mediterranean, summer dormancy is the main feature of the seasonal dynamics of many benthic suspension feeders. A common characteristic
of all Mediterranean aestivation taxa is a marked decrease in investment in secondary production (i.e. growth and
reproduction) during the summer period. However, the aestivation process differs widely among taxa, ranging from
the regression of whole colonies (hydrozoans) to constraints only on certain biological functions (bivalvia and anthozoa). Decreased abundance can be observed in most hydrozoans and colonial ascidians in summer. During this
period, most of the hydrozoan species remain in the form of dormant stolons6. Most colonial ascidians also undergo
a decrease in abundance or disappear entirely in summer, although it is unclear whether these species have one
generation per year or are pluriannual and remain unidentifiable as resistance forms during summer. Changes in
abundance do not occur in anthozoans, where aestivation processes are characterized by a decrease in investment
in secondary production and in feeding activity during the summer period12, and some species exhibit nonfeeding
periods during which the surface of the whole colony becomes covered by a glassy cuticle13. Nonfeeding periods are
also exhibited by some colonial ascidians, in which two main patterns have been described. The first is the onset of
survival budding, with the thorax becoming inactive and regressing, and the abdomen and postabdomen filling with
reserve substances (e.g. Pseudodistoma crucigaster). The second is the development of a glassy pellicle that covers
the entire colony and seals the siphonal apertures (e.g. Polysyncraton lacazei ). These different processes allow taxa
exhibiting aestivation to withstand the adverse conditions of the summer period in the Mediterranean.
The presence of resting stages is a common mechanism in marine organisms. Resting stages of some taxa can
remain inactive for long periods and can act as biodiversity reservoirs. Several recent studies into the role of resting stages have contributed to a recognition of the importance of life cycle dynamics in structuring marine communities by contributing to explain fluctuations not only in benthic communities but also in phyto- and zooplankton
communities36,37.
450
competition in determining
seasonal patterns needs further investigation. However,
algal abundance drops off
sharply in summer. An
energy shortage has been
suggested as the main reason why hydrozoan populations do not increase abundance even though algal
communities are no longer
prevalent in summer12.
Nevertheless, many taxa do
not experience declining
abundance in spring but
rather curtail activity in summer. Space competition with
algae does not furnish an
explanation for aestivation
processes in anthozoans and
other taxa.
Temperature and food
availability have both been
identified as crucial environmental factors affecting the
dynamics of benthic suspension feeders throughout the
year. In cold temperate
waters, seasonal changes
in physiological processes
have usually been related to
temperature variations. Food
availability is low during the
winter in cold temperate
seas because of the inhibition of phytoplankton
growth resulting from the
increased depth of the mixed
layer and low irradiance.
However, studies of food
availability are scarce. An
intrinsic feature of cold temperate ecosystems is that
temperature and food availability tend to be positively
correlated22, thus making it
difficult to distinguish the
relative importance of these
two effects. This has constrained evaluation of the
importance of food availability. However, studies on benthic suspension feeders conducted in the past decade
suggest that food availability
could be as important as
temperature in determining
seasonality in marine organisms12,23,24.
In the Mediterranean,
winter cooling produces a
breakdown of the thermocline and the subsequent vertical mixing brings nutrients
to the surface from the deep
water. Phytoplankton blooms
occur in winter– spring when
TREE vol. 15, no. 11 November 2000
REVIEWS
surface waters begin to stabilize, and in autumn at the
Warm temperate – no aestivation
beginning of the mixing
period25. This alternation of
Ascidiacea
Microcosmus sabatieri
stratified and mixing periods
Halocynthia papillosa
confers strong seasonality to
primary production. High
Crambe crambe
Porifera
irradiance in the summer is
also conducive to strong
Mycale contarenii
stratification of the water colTethya aurantium
umn and wind action homogenizes the top layer by its
Tethya citrina
turbulence. The stratification
of the water column enJ
F
M
A
M
J
J
A
S
O
N
D
hances both particle sinking
and nutrient exhaustion, thus
Winter
Spring
Summer
Autumn
resulting in severe depletion
of suspended materials durGrowth
Asexual reproduction
Sexual reproduction
Toxicity
ing the Mediterranean summer. Therefore, the intrinsic
Trends in Ecology & Evolution
feature of cold temperate ecosystems – that temperature
Fig. 3. Data on the annual activity patterns (i.e. secondary production and activity) of benthic suspension feeders
and food availability tend to
from different taxa not exhibiting aestivation (summer dormancy) in the warm temperate Mediterranean.
Compiled from Refs 14,16,18,19.
positively correlate22 – does
not occur in Mediterranean
ecosystems.
In different taxa, researchers have found that summer withstand the normal duration of adverse summer conis an unfavourable season for Mediterranean benthic sus- ditions but not an anomalous prolongation of these conpension feeders5,8,12 and that an energy shortage could be ditions. However, lack of knowledge about the effects of
the cause of aestivation12. Benthic suspension feeders are temperature variation on physiological processes in
entirely dependent on the supply of food that reaches their Mediterranean benthic suspension feeders still limits
capture organs. Thus, the depletion of suspended ma- our understanding of the factors that constrain their
terials during the summer period is consistent with these dynamics.
results. Reduced resources, high water column stability
Several small-scale mass mortality events have been
and high temperatures are the main characteristics of the recorded during the past decade in the Mediterranean28.
summer condition. However, we do not have enough These small-scale events, together with the occurrence of
knowledge about the natural diets of benthic suspension the large-scale event in 1999, suggest that they might be
feeders and about the fluctuation in food availability to related to seawater temperature increase and global warmform a clear picture of the trophic dynamics in this system. ing. Although a warming trend might be clear in deep
In the Mediterranean, temperature can fluctuate by water, some evidence indicates that the weak warming of
approximately 108C throughout the year – this can have the sea surface might be part of an oscillation29. Further
important consequences for the metabolism of benthic sus- research is needed to understand the dynamics of seapension feeders. Nevertheless, there is only one respiration water temperature and the consequences of small changes
study conducted seasonally26, which has showed a positive on the performance of the climate, seawater circulation
correlation between temperature and respiration rate, and and hydrographic characteristics. Nevertheless, whether
has provided an estimated Q10 of 2.37. This increase in respi- the mass mortality event is related to global warming or is
ration rate should affect the energy budget of the species by
reducing the energy available for other activities. However,
Box 2. Seasonal dynamics of benthic algal
patterns to reduce the temperature dependence of respicommunities
ration have been reported in extreme environments. For
example, the respiration rate in Antarctic ecosystems is
Algal communities are fundamental components of benthic communities
between the surface and about 60 m in depth. Several well differentiated
higher than expected for the habitat temperature27. Metaalgal communities can be distinguished along this depth range. The depth
bolic responses of organisms to temperature might also
range inhabited by each community can vary locally as a function of water
depend on food availability because, in species suffering
quality and orientation. Seasonal changes in algal abundance are common in
from a food shortage, metabolic adjustments to reduce
temperate seas. In the Mediterranean, seasonal changes in algal abundance
energy losses could be crucial. In this sense, an energy
significantly affect community structure. Temporal availability of light and
nutrients are the main factors determining the production of algal commushortage, as a result of reduced resources and high temnities. However, because seasonal light availability values (highest in sumperatures, might be related to the mass mortality event of
mer and lowest in winter) contrast with nutrient values (highest in winter and
benthic suspension feeders that occurred in the summer
lowest in summer)38, the dynamics of algae from different groups and
of 1999 (Ref. 28). Owing to climatic and hydrographic
depths adapt to the seasonal cycle of the main limiting factor affecting them.
In this sense, nutrients are the primary limiting factor for shallow-water
anomalies on the Ligurian Sea (Northwestern Mediteralgae, whereas light is the most limiting factor for deep-water algae. This
ranean), the characteristic summer conditions of reduced
results in a temporal lag in algal community production peaks with depth.
resources, high water column stability and high temperaAlgal community production peaks occur in spring in shallow communities
tures (normally during July and August) lasted much
and in summer in deep communities38. Nevertheless, the highest algal prolonger than usual (until October). This coincided with a
duction levels are observed in shallow water, where the significant seasonal
changes in algal abundance strongly affect community structure.
mass mortality event of benthic suspension feeders over
several hundred kilometres. Organisms might be able to
TREE vol. 15, no. 11 November 2000
451
REVIEWS
Box 3. The Antarctic Ocean
The annual temperature in the Antarctic Ocean ranges between approximately 1.88C and 2.08C. This low, but relatively stable, temperature, combined with a brief and intense period of open water phytoplankton productivity, offers another system where the annual variation in temperature and
food availability does not correlate1. Studies in Antarctic systems have been
restricted mainly to summer periods as a result of logistic constraints. However, during the past few years, the need for year round studies of Antarctic
ecosystems has been emphasized to obtain a complete understanding of
their function.
Benthic suspension feeders in the Antarctic Ocean exhibit marked variation in secondary production throughout the year39. To double the rate of
secondary production by an increase in 28C would imply a Q10 for secondary
production of 32 or more – values outside 1–5 are unusual1. Thus, annual
changes in secondary production cannot be attributed to temperature variation alone, as they have usually been related in cold temperate systems4.
The restriction of studies to the summer months and the marked summer
peak of phytoplankton lead to the hypothesis that benthic suspension feeders are subjected to a long period of starvation owing to reduced resources
and water movement in the winter. This view is based on studies of phytoplankton, but microplankton were evaluated as the main primary source of
energy for the system. However, the recent development of flow cytometry
and related techniques has highlighted the problems in examining energy
flux without considering microbial communities. In the Antarctic Ocean,
90% of the total chorophyll resides in pico- and nanoplankton, with diatoms
and dinoflagellates contributing little40. Furthermore, the duration of picoand nanoplankton blooms exceeds that of microplankton41.
Recent studies have examined the feeding activity of a wide variety of benthic suspension feeders, such as bryozoans, hydrozoans, polychaetes and
holothurians, throughout the entire year. These studies show that most
groups exhibit a period of reduced feeding, which is shorter than the winter,
and suggest that changes in water column chlorophyll appear to be the main
environmental cue for changes in benthic feeding activity23. The period of
feeding cessation for most benthic taxa coincides with the low concentration
of nanoplankton in winter. Thus, there appears to be a coupling between food
availability and the seasonal pattern of feeding, polypide cycling (the retractile
portion of the zooid of bryozoans, which is transient) and sexual reproduction
of benthic suspension feeders42. This coupling suggests that taxa that use
mainly microplankton as a resource, such as holothurians, might have brief
periods of activity and growth, although taxa that use nanoplankton might have
large periods of activity and growth23.
a periodic, but infrequent, event is still unclear. The study
of long-lived organisms that exhibit records of changes in
their structures might contribute to the resolution of this
issue. In either case, owing to the low dynamics of Mediterranean benthic suspension feeder communities9,12,13,16, the
occurrence of mass mortality events can strongly affect
benthic community composition in littoral waters. If mass
mortality events are related to the global warming trend of
the NW Mediterranean, these events might occur again and
become more frequent, which would induce profound
changes in the present benthic community composition in
littoral areas. Long-term studies are needed to properly
evaluate resilience or changes in community composition.
Recognition that food can play a major role in the
function and dynamics of benthic suspension feeders has
not been restricted to the Mediterranean. Several recent
studies on feeding activity in benthic suspension feeders in
the Antarctic Ocean suggest that variation in resource
availability acts as the main cue for their seasonal patterns
(Box 3). Seasonal resource limitation does appear to be
important in some ecosystems, such as the Mediterranean
and the Antarctic Ocean, and food constraints might have
a large effect on the life histories of some species and
taxa12,23,24. In this sense, seasonality in deep-sea habitats is
mainly regulated by periodic inputs of particulate organic
matter that sinks from the euphotic zone or occurs by lateral advection30. In addition, energy inputs are the main
factor determining seasonal biological rhythms in open regions31. Energy supplied by the seasonal cycle of irradiance
452
forces photosynthesis and water stratification, and local
wind and precipitation regimes force water mixing and
nutrient transfer.
The seasonal cycle of primary productivity and
temperature in the Mediterranean resembles that of
other warm temperate areas, such as the subtropical
Atlantic31. Research in other warm temperate areas would
establish whether the seasonal pattern observed in the
Mediterranean is characteristic of benthic suspension
feeder dynamics in most warm temperate seas throughout
the year.
Research priorities
Advances in our knowledge of benthic ecosystems at broad
scales can obtain little benefit from certain technical advances (such as satellite images, but see remote sensing)
that have allowed a rapid advance in our understanding of
the functioning of neritic ecosystems worldwide31. Knowledge must advance by contributions from detailed empirical studies; this constraint makes generalizations difficult
because the number of available examples is usually limited. Thus, although there is now ample evidence that
some Mediterranean benthic suspension feeders exhibit a
seasonal pattern, characterized by aestivation, further
studies of seasonal patterns are needed to assess whether
summer dormancy is a widespread phenomenon in warm
temperate ecosystems.
The study of species with distribution ranges large
enough to be exposed to variation in dominant environmental factors (such as a species with Atlantic–Mediterranean
distribution) would allow examination of differences in
seasonal patterns of benthic suspension feeders in both
cold and warm temperate ecosystems.
Present technological advances in flow cytometry and
related techniques have substantially reduced the effort
required to perform analysis of seasonal variation in the
entire spectrum of potential water column food sources, as
well as to conduct natural feeding studies. These studies
are crucial for understanding the functioning and dynamics
of coastal marine ecosystems worldwide.
Water motion is a fundamental factor influencing all
aspects of the life cycles of benthic suspension feeders.
However, knowledge about variability in water motion
throughout the year at the organism scale, as well as about
the response of the organism to these changes, is still limited. Significant efforts to understand the effects of water
movement on prey capture and on metabolism have been
conducted32,33. Further studies are needed to understand
the mechanisms underlying the aestivation phenomenon,
to obtain accurate measurements of total ingestion and to
evaluate the impact of benthic suspension feeders on
planktonic communities.
In the Antarctic Ocean, annual temperature variation is
so small that the effects of temperature change appear to
be of little significance1. This is not the case for warm temperate seas, such as the Mediterranean, where temperature variation can have important consequences for the
metabolism of benthic suspension feeders, and, therefore,
where respiration studies are needed to evaluate the
effects of temperature. These studies should be conducted
in situ and should consider seasonal patterns in secondary
production of the species, because secondary production
can strongly affect respiration. The fact that secondary
production of many taxa is not correlated with temperature makes the Mediterranean environment a convenient
ecosystem in which to distinguish the effects of secondary
production from those of temperature.
TREE vol. 15, no. 11 November 2000
REVIEWS
Environmental factors, such as photoperiod, light intensity, food availability, oxygen, salinity and temperature, all
influence energy expenditure in marine organisms. Generally, organisms react to their total environment rather than
to a single factor. Therefore, a combination of environmental factors would provide the most successful approach to
understanding seasonal patterns of benthic suspension
feeders. It will be a challenge to integrate the effects of
multiple factors, as well as their interactive effects, to
determine seasonality in the life cycles of marine organisms.
Acknowledgements
This article was improved by the comments of R.A. Kinzie III,
E. Cox, F. Boero and J.D. Ros. We would like to thank A. Clarke
who sent us helpful papers. We acknowledge the assistance of
J.M. Llenas, E. Pola, D. Diaz and S. Rossi, and thank Point Lab
(Hawaii Institute of Marine Biology) for valuable discussions.
Support for this work was provided by a RED research contract
from the Generalitat de Catalunya to R.C., by Postdoctoral
Fellowship from the Ministerio de Educación y Cultura to M.R.,
by the UE-MAST-III-ELOISE METRO MED Project and by the
ERB MAS3-CT97-0155-ECOMARE concerted action.
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