The effect of extreme climatic events on littorinid snails in two estuarine environments, temperate (NW Spain) and tropical (NE Brazil)
DOI:
https://doi.org/10.1590/Keywords:
Brazil, Climate change, Desiccation, Littoraria, Littorina, SpainAbstract
Extreme weather events (e.g., droughts, excessive precipitation) are expected to increase in frequency and
severity in the coming decades due to climate change, causing significant impacts on society and ecosystems.
Because these events are rare and complex, they have been studied with manipulative experiments. Littorinidae
snails inhabit a complex and variable environment in which they must deal with periodic extreme events and
are thus considered excellent ecological models for these studies. Therefore, this study aimed to understand
the effects of extreme climatic events on the survival and weight of the species Littorina fabalis and Littorina
littorea in Spain and Littoraria angulifera and Littoraria flava in Brazil. Higher mortality rates and greater weight
loss were observed in the desiccation resistance treatment compared to the control treatment in both countries.
The results showed dependence on the species’ body size. The submergence tolerance treatment indicated
that the species from Spain are more susceptible to mortality in response to excessive rainfall and/or coastal
flooding. Each species tested for the effect of extreme climatic events using an integrated response strategy
with clear latitudinal differences. Understanding the organisms’ responses at different latitudes is essential for
conservation biology on a global scale.
References
Boehs, G. & Freitas, L. A. 2022. Population attributes
of Littoraria angulifera (Gastropoda: Littorinidae) in
mangroves in Bahia State, northeastern Brazil. Brazilian
Journal of Biology, 82, e243114. DOI: https://doi.
org/10.1590/1519-6984.243114
Boersma K. S., Nickerson, A., Francis, C. D. & Siepielski,
A. M. 2016. Climate extremes are associated with
invertebrate taxonomic and functional composition in
mountain lakes. Ecology and Evolution, 6, 8094–8106.
DOI: https://doi.org/10.1002/ece3.2517
Bosso, L., Smeraldo, S., Russo, D, Chiusano, M. L.,
Bertorelle, G., Johanneson, K., Butlin, K., Danovaro, R.
& Raffini, F. 2022. The rise and fall of an alien: why the
successful colonizer Littorina saxatilis failed to invade
the Mediterranean Sea. Biological Invasions, 24, 3169-
DOI: https://doi.org/10.1007/s10530-022-02838-y
Brahim, A., Mustapha, N. & Marshall, D. J. 2018. Nonreversible and Reversible Heat Tolerance Plasticity
in Tropical Intertidal Animals: Responding to Habitat
Temperature Heterogeneity. Frontiers in Physiology, 9,
-11. DOI: https://doi.org/10.3389/fphys.2018.01909
Britton, J. C. 1992. Evaporative water loss, behaviour
during emersion, and upper thermal tolerance limits
in seven species of eulittoral-fringe Littorinidae
(Mollusca: Gastropoda). In: International Symposium
on Littorinidae Biology (3 ed, pp. 69–83).
Cacabelos, E., Gestoso, L. & Troncoso, J. S. 2008.
Macrobenthic fauna in the Ensenada de San
Simón (Galicia, north-western Spain). Journal of
the Marine Biological Association of the United
Kingdom, 88, 237-245. DOI: https://doi.org/10.1017/
S0025315408000660.
Capaldo, P. S. 1983. Tolerance of the common marsh
snail Melampus bidentatus to submersion. Estuaries,
, 176–177.
Chapman, M. G., 1997. Relationships between shell
shape, water reserves, survival and growth of
highshore Littorinids under experimental conditions
in New South Wales, Australia. Journal of Molluscan
Studies, 63, 511–529.
Darnell, M. Z. & Darnell, K. M. 2018. Geographic variation
in thermal tolerance and morphology in a fiddler crab
sister-species pair. Marine Biology, 165, 26. DOI: https://
doi.org/10.1007/s00227-017-3282-y
Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon,
S. A., Karl, T. R. & Mearns, L. O. 2000. Climate
Extremes: Observations, modeling, and impacts.
Science, 289, 2068-2074. https://doi.org/10.1126/
science.289.5487.2068
FUNCEME (Fundação Cearense De Meteorologia E
Recursos Hídricos). 2018. Posto meteorológico de
Acaraú. Availablr from: www.funceme.br. Acess date:
feb. 2024.
Iacarella, J. C. & Helmuth, B. 2011. Experiencing the salt
marsh environment through the foot of Littoraria irrorata:
Behavioral responses to thermal and desiccation
stresses. Journal of Experimental Marine Biology and
Ecology, 409, 143-153. DOI: https://doi.org/10.1016/j.
jembe.2011.08.011
Stocker, T. F., Qin, D., Plattner, G.-K., Tignor, M., Allen,
S. K., Boschung, J., Nauels, A., Xia, Y., Bex, V. &
Midgley, P. M. (eds.). 2013. Climate Change: The
Physical Science Basis. Cambridge, Cambridge
University Press.
Jentsch, A., Kreyling, J. & Beierkuhnlein, C. 2007. A new
generation of climate-change experiments: Events,
not trends. Frontiers in Ecology and the Environment,
, 365-374. DOI: https://doi.org/10.1890/1540-
(2007)5[365:ANGOCE]2.0.CO;2
Leeuwis R., H. J. & Gamperl, A. K. 2022. Adaptations and
plastic phenotypic responses of marine animals to the
environmental challenges of the high intertidal zone.
Oceanography and Marine Biology: An Annual Review,
, 625-680.
Liao M. L., Zhang, S., Zhang, G. Y., Chu, Y. M., Somero,
G. N. & Dong, Y. W. 2017. Heat-resistant cytosolic
malate dehydrogenases (cMDHs) of thermophilic
intertidal snails (genus Echinolittorina): protein
underpinnings of tolerance to body temperatures
reaching 55°C. Journal of Experimental Biology, 220,
-2075. DOI: https://doi.org/10.1242/jeb.156935
Maia, R. C. & Coutinho, R. 2012. Structural characteristics
of mangrove forest in Brazilian estuaries: A comparative
study. Journal of Marine Biology and Oceanography,
, 87-98.
Maia, R. C. & Troncoso, J. S. 2022. Evaluation of the
synergistic effects of climate change on estuarine
ecosystems at temperate and tropical latitudes using
Littorinids (Mollusca: Gastropoda) as indicators.
Brazilian Journal of Animal and Environmental
Research, 5, 1642-1660.
Marshall, D. J., Baharuddin, N. & Mcquaid, C. D. 2013.
Behavior moderates climate warming vulnerability in
high-rocky-shore snails: interactions of habitat use,
energy consumption and environmental temperature.
Marine Biology, 160, 2525–2530. DOI: https://doi.
org/10.1007/s00227-013-2245-1.
Marshall, D. J., Brahim, A., Mustapha, N., Dong, Y.
& Sinclair, B. J. 2018. Substantial heat tolerance
acclimation capacity in tropical thermophilic snails, but
to what benefit? Journal of Experimental Biology, 221,
jeb187476. DOI: https://doi.org/10.1242/jeb.187476
Marshall D. J., Mcquaid, C. D. & Williams, G. A. 2010.
Non-climatic thermal adaptation: Implications for
species’ responses to climate warming. Biology
Climate change impacts on littorinid snails
Ocean and Coastal Research 2024, v72(suppl 1):e24017 12
Maia and Troncoso
Letters, 6, 669–673. DOI: https://doi.org/10.1098/
rsbl.2010.0233
Matos, A., Matthews-Cascon, H. & Chaparro, O. 2020.
Morphometric analysis of the shell of the intertidal
gastropod Echinolittorina lineolata (d’Orbigny, 1840)
at different latitudes along the Brazilian coast. Journal
of the Marine Biological Association of the United
Kingdom, 100, 725-731. DOI: https://doi.org/10.1017/
S0025315420000624
Mcquaid, C. D. 1996a. Biology of the gastropod Family
Littorinidae: I. Evolutionary aspects. Oceanography and
Marine Biology: An Annual Review, 34, 233-262.
Mcquaid, C. D. 1996b. Biology of the gastropod Family
Littorinidae: II. Role in the ecology of intertidal and
shallow marine ecosystems. Oceanography and Marine
Biology: An Annual Review, 34, 263-302.
Mcmahon, R. F. 1988. Respiratory Response to Periodic
Emergence in Intertidal Molluscs. American Zoologist,
, 97-114.
Moreno, J. & Møler, A. P. 2011. Extreme climatic events
in relation to global change and their impact on life
histories. Current Zoology, 57, 375-389. DOI: https://
doi.org/10.1093/czoolo/57.3.375
Monjo, R., Gaitán, E., Pórtoles, J., Ribalaygua, J. & Torres, L.
Changes in extreme precipitation over Spain using
statistical downscaling of CMIP5 projections. International
Journal of Climatology, 36, 757–776. DOI: https://doi.
org/10.1002/joc.4380
Moutinho, P. R. S. & Alves-Costa, C. P. 2000. Shell size
variation and aggregation behavior of Littoraria flava
(Gastropoda: Littorinidae) on a Southeastern Brazilian
shore. Veliger, 43, 277–281.
Ng, T. P. T., Davies, M. S., Stafford, R. & Williams, G. A.
Mucus trail following a mate-searching strategy
in mangrove littorinid snails. Animal Behavior, 82, 459-
DOI: https://doi.org/10.1111/brv.12023
Ng, T. P.T., Laua, S. L. Y, Seuront, L., Davies, M. S.,
Staffordd, R., Marshall, D. J. & Williams, G. A. 2017.
Linking behavior and climate change in intertidal
ectotherms: insights from littorinid snails. Journal of
Experimental Marine Biology and Ecology, 492, 121-131.
DOI: https://doi.org/10.1016/j.jembe.2017.01.023
Parada, J. M., Molares, J. & Otero, X. 2012. Multispecies
Mortality Patterns of Commercial Bivalves in Relation to
Estuarine Salinity Fluctuation. Estuaries and Coasts, 35,
-142. DOI: https://doi.org/10.1007/s12237-011-9426-2
Perez-Arlucea, M., Mendez, G., Clemente, F., Nombela,
M., Rubio, B. & Filgueira, M. 2005. Hydrology, sediment
yield, erosion and sedimentation rates in the estuarine
environment of the Ría de Vigo, Galicia, Spain. Journal
of Marine Systems, 369, 79-86. DOI: https://doi.
org/10.1016/j.jmarsys.2004.07.013
Reid, D. G. 1996. Systematics and Evolution of Littorina.
London, Ray Society.
Reid, D. G., Dyal, P. & Williams, S. T. 2009. Global
diversification of mangrove fauna: a molecular
phylogeny of Littoraria (Gastropoda: Littorinidae).
Molecular Phylogenetics and Evolution, 55, 185–201.
DOI: https://doi.org/10.1016/j.ympev.2009.09.036
Reid, D. G. 1989. Comparative morphology, phylogeny
and evolution of the gastropod family Littorinidae.
Philosophical Transactions of the Royal Society of
London, Series B, 324(1220), 1-110. DOI: https://doi.
org/10.1098/rstb.1989.0040
Robins, P. E., Skov, M. W., Lewis, M. J., Gimenez, L., Davies, A.
G., Malham, S. K., Neill, S. P., Mcdonald, J. E., Whitton, T. A.,
Jackson, S. E. & Jago, C. F. 2016. Impact of climate change
on UK estuaries: A review of past trends and potential
projections. Estuarine, Coastal and Shelf Science, 169,
-135. DOI: https://doi.org/10.1016/j.ecss.2015.12.016
Rolán-Alvarez, E., Austin, C. J. & Boulding, E. G. 2015.
The contribution of the genus Littorina to the field
of evolutionary ecology. Oceanography and Marine
Biology: An Annual Review, 53, 157-214. DOI: https://
doi.org/10.1201/b18733-6.
Scheffers B. R., Edwards, D. P., Stephen, A. D., Williams,
E. & Evans, T. A. 2014. Microhabitats reduces animal’s
exposure to climate extremes. Global Change Biology,
, 495-503. DOI: https://doi.org/10.1111/gcb.12439
Sergio, F., Blas, B. & Hiraldo, F. 2018. Animal responses
to natural disturbance and climate extremes: a review.
Global and Planetary Change, 161, 28-40. DOI: https://
doi.org/10.1016/j.gloplacha.2017.10.009
Smith, M. D. 2011. An ecological perspective on extreme
climatic events: a synthetic definition and framework to
guide future research. Journal of Ecology, 99, 656–663.
DOI: https://doi.org/10.1111/j.1365-2745.2011.01798.x
Sheridan, J. A. & Bickford, D. 2011. Shrinking body
size as an ecological response to climate change.
Nature climate change, 1, 401-406. DOI: https://doi.
org/10.1038/nclimate1259
Tanaka, M. O. & Maia, R. C. 2006. Shell Morphological
Variation of Littoraria angulifera among and within
mangroves in NE Brazil. Hydrobiologia, 559, 193-202.
Vermeij, G. J. 1972. Intraspecific shore level size gradients
in intertidal mollusks. Ecology, 53, 693–700.
Vinagre, C., Leal, I., Mendonça, V., Madeira, D., Narciso,
L., Diniz, M. S. & Flores, A. A. V. 2015. Vulnerability
to climate warming and acclimation capacity of
tropical and temperate coastal organisms. Ecological
Indicators, 62, 317-327. DOI: https://doi.org/10.1016/j.
ecolind.2015.11.010
Vinagre, C., Leal, I., Mendonça, V., Cereja, R., AbreuAfonso, F., Dias, R., Mizrahi, D. & Flores, A. A. V.
Ecological traps in shallow coastal waters -
Potential effect of heat-waves in tropical and temperate
organisms. Plos one, 13, e0192700. DOI: https://doi.
org/10.1371/journal.pone.0192700
Wernberg, T., Smale, D. A. & Thomsen, M. S. 2012.
A decade of climate change experiments on marine
organisms: procedures, patterns and problems. Global
Change Biology, 18, 1491-1498. DOI: https://doi.
org/10.1111/j.1365-2486.2012.02656.x
Wetz, M. S. & Yoskowitz, D. W. 2013. An ‘extreme’ future
for estuaries? Effects of extreme climatic events on
estuarine water quality and ecology. Marine Pollution
Bulletin, 69, 7-18. DOI: https://doi.org/10.1016/j.
marpolbul.2013.01.020
Zajac, R., Kelly, E., Perry, D. & Espinosa, I. 2017. Population
ecology of the snail Melampus bidentatus in changing
salt marsh landscapes. Marine Ecology, 38, 1-17. DOI:
