Biol. Mar. Mediterr. (2010), 17 (1): 116-118
N. Rauh1,2, C. Brownlee2, S.J. Hawkins3, A.M. Hetherington2
The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, U.K.
[email protected]
2
Universtiy of Bristol, United Kingdom.
3
University of Bangor, Wales.
1
HYPO-OSMOTIC STRESS TOLERANCE AMONG THREE
INTERTIDAL FUCUS SPECIES: EFFECTS ON SURVIVAL,
RECRUITMENT AND COMMUNITY COMPOSITION
TOLLERANZA ALLO STRESS IPOOSMOTICO IN TRE SPECIE
INTERTIDALI DI FUCUS: EFFETI SU SOPRAVIVENZA,
RECLUTAMENTO E COMPOSIZIONE DELLA COMUNITÀ
Abstract – These studies aimed to test the extent to which the distribution of fucoid algae is
determined by recruitment and survival of early developmental stages (zygotes and embryos); in
particular the influence of abiotic (osmotic) stress at early development stages on subsequent growth
and survival. Comparative physiological experiments have been carried out on three dominant fucoid
species native to the UK. A further investigation into the acute responses to hypo-osmotic treatment,
has shown that embryos are susceptible to osmotic stress caused both by exposure to rainfall at low tide
and re-immersion into seawater following periods of desiccation. This work has also shown that zygotes
and embryos of the three most common fucoid species (Fucus spiralis, F. vesiculosus and F. serratus)
display dramatically different physiological strategies for tolerating osmotic stress.
Key-words: Ecological zonation, osmotic pressure, seaweed embryo.
Introduction - Temperate rocky shore habitats comprise complex interacting
physical gradients and show temporal fluctuations in a number of environmental
variables (Stephenson & Stephenson, 1949; Lewis, 1964). The varying levels of
stress associated with these gradients and fluctuations contribute to the competitive
interactions between organisms in this habitat (Baker, 1909, 1910; Davison &
Pearson, 1996). On the other hand, physical heterogeneity creates numerous potential
ecological niches that may underlie both high biodiversity and biomass (Helmuth &
Hofmann, 2001). Hypo-osmotic stress is likely to be encountered with every tidal
cycle, either through sporadic events of rainfall or re-immersion into seawater
following periods of desiccation. The resistance to physical stress of fucoid algae
has previously been demonstrated through adaptive mechanisms within established
adult populations (Chapman, 1995; Davison & Pearson, 1996). However, this has not
been fully examined in early developmental stages, such as zygotes and embryos
that are potentially exposed to the same physical factors as adults and are likely to
be more vulnerable to stresses. Higher shore levels experience exposure to emersion,
specifically osmotic, stresses more frequently and for longer periods of time than
lower shore levels (Stephenson & Stephenson, 1949). We have demonstrated that
zygotes and embryos of Fucus species from higher shore levels display very different
physiological strategies for tolerating osmotic stress than neighbouring species lower
down the shore gradient. We have developed new approaches to monitor fucoid
propagule supply and recruitment in situ. Field studies reveal that physiological
tolerance mechanisms identified from laboratory experiments have real ecological
relevance in terms of survival, recruitment, and community.
Materials and methods – Experiments characterising physiological parameters
were designed to examine individual tolerance, adaptive mechanisms and ecological
relevance in the field.
Hypo-osmotic stress tolerance among three intertidal Fucus species
117
Tolerance: Cell burst assays recorded species survival following exposure to a
severe (10‰ S) hypo-osmotic treatment throughout the first 48h of development.
Species survival was assessed following a period of induced desiccation and
re-immersion into natural seawater.
Adaptive Mechanisms: Cell volume measurements monitored volumetric changes
occurring within zygotes during and immediately after mild (15‰ S) hypo-osmotic
exposure. Sub-lethal effects of hypo-osmotic exposure were tested by exposing
zygotes to several dilute salinity concentrations over varying lengths of exposure
time, measuring the ratio between length/width growth over seven days.
Field studies: involved both manipulative and descriptive experiments.
Manipulative experiments transplanted laboratory released zygotes to high, mid and
low shore levels for 24h. Descriptive sampling monitored the supply of propagules
versus percentage recruitment. Wild fucoid embryos were identified to species level
using a pioneered technique relying on auto-fluorescence using confocal microscopy
and ratio image analysis identification.
Results – Tolerance: Resistance to hypo-osmotic shock varied throughout
development in all three fucoid species. Inter-specific differences in tolerance were
also apparent. Embryos of the high shore alga, Fucus spiralis, as expected burst
significantly less than the mid shore, F. vesiculosus, and low shore, F. serratus,
embryos respectively when given the same hypo-osmotic treatment. Fucoid embryos
also encountered hypo-osmotic stress after a period of desiccation followed by
re-immersion to seawater. Bursting was highest among embryos from the low shore
(F. serratus) with survival increasing respectively in F. vesiculosus and then F. spiralis.
Adaptive Mechanisms: To examine mechanisms, we looked at volume control during
mild stress exposure the high shore alga, F. spiralis, exerted considerable control over
its internal volume preventing rhizoid apex swelling. However, when re-immersed
in natural (34‰ S) seawater, F. spiralis expressed ion loss as a function of drastic
rhizoid shrinking. The mid shore species, F. vesiculosus, demonstrated negligible
fluctuations to its internal volume both during exposure and following re-immersion
to seawater, no significant swelling or shrinking. The low shore species, F. serratus,
possessed little internal volumetric control, swelling considerably during exposure
and once re-immersed returned to a volume comparable prior to exposure. Burst
characterisation indicated that the mid shore species, F. vesiculosus, possesses a high
internal pressure despite not swelling prior to bursting, suggesting that cell walls
may be reinforced in a thickening process. Assessing the sub-lethal effects following
various exposure regimes, higher shore species (F. spiralis and F. vesiculosus) exhibited
a negative response in terms of length/width growth compared to low shore species
(F. serratus).
Field studies: Manipulative field sampling showed survival to be highest among
higher shore species, F. spiralis and F. vesiculosus, and lowest survival recorded
among low shore species, F. serratus at all shore levels. Wild embryos of all three
Fucus species could be identified on the basis of their autofluorescence properties.
Descriptive field sampling indicated a significant export of low shore species’ (F.
serratus) propagules to higher shore levels; similarly higher shore species’ (F. spiralis
and F. vesiculosus) propagules were also being supplied to lower shore levels. Higher
shore species exhibit a similar recruitment success at all shore levels. However,
F. serratus (low shore) propagules exhibited a declining recruitment success with
increasing shore height.
Conclusions - Closely related fucoid species demonstrate very different osmotic
strategies to optimise survival within natural shore position. The high shore fucoid,
118
N. Rauh, C. Brownlee, S.J. Hawkins, A.M. Hetherington
Fucus spiralis, possesses a higher tolerance to hypo-osmotic stress through the
development of an intricate osmo-regulatory mechanism. This mechanism comes at
a price to growth and competitive ability likely to be responsible for its inability to
significantly colonise lower shore levels. The mid shore fucoid, F. vesiculosus, does
not seem to possess an osmo-regulatory mechanism; instead it is likely to rely on
structural reinforcement through thicker cell walls conferring tolerance. The low
shore fucoid, F. serratus, a passive osmometer, invests little energy into tolerating
hypo-osmotic stress and as a result is less capable of recruiting outside its natural
shore position on higher shore levels. There is an indication that greater exposure on
higher shore levels contributes to a higher tolerance of fluctuations in the external
osmotic environment. Hypo-osmotic stress is a likely significant selective pressure
acting negatively on vulnerable early developmental stages in recruiting fucoid algae,
contributing to community composition.
References
BAKER S.M. (1909) - On the causes of zonation of brown seaweeds on the seashore. New
Phytologist, 8: 196-202.
BAKER S.M. (1910) - On the causes of the zonation of brown seaweeds on the seashore II. The
effect of periodic exposure on the expulsion of gametes and in the germination of the oospore.
New Phytologist, 9: 54-67.
CHAPMAN A.R.O. (1995) - Functional Ecology of Fucoid Algae - 23 Years of Progress. Phycologia,
34: 1-32.
DAVISON I.R., PEARSON G.A. (1996) - Stress tolerance in intertidal seaweeds. J. Phycol., 32:
197-211.
HELMUTH B.S.T., HOFMANN G.E. (2001) - Microhabitats, thermal heterogeneity, and patterns
of physiological stress in the rocky intertidal zone. Biol. Bull., 201: 374-384.
LEWIS J.R. (1964) - The ecology of rocky shores. Vol. English Universities Press, London.
STEPHENSON T.A., STEPHENSON A. (1949) - The universal features of zonation between the
tidemarks on rocky coasts. J. Ecol., 38: 289-305.