Climate Change and Sponges: An Introduction

Abstract

This chapter provides an introduction to our current understanding of the two most important features of climate change affecting marine sponges—ocean warming and ocean acidification. Of these two stressors, thermal stress associated with ocean warming is likely to have the greatest influence on the sponge assemblages through the induction of diseases and mortality by a decrease in the efficacy of defense mechanisms and development of pathogens. However, there is a considerable variability among species in their responses to increasing temperature, and some species have persisted during episodes of unusually high temperature. Conspicuous sublethal effects have also been described. Thermal stress can limit sponge reproductive capability and dispersal by causing the reabsorption of spermatic cysts and oocytes and by the disruption of the feedback mechanism that prevents the release of asexual propagules when ecological factors are unsuitable for propagule survival. Thermal stress also can affect sponge-feeding behavior by increasing or decreasing filtration rates and by decreasing choanocyte chamber density and size, causing shifts in the microbial communities of the host sponge, and can also increase the production of heat shock proteins, which leads to rapid upregulation of genes involved in cellular damage repair. The effects of ocean acidification on sponges are much less known, but recent studies have demonstrated the resistance of certain species to lowered pH conditions. It seems that this capacity to withstand OA lies in part in the ability of sponges to restructure their host-associated microbiomes mainly by acquiring new microbial components via horizontal transmission. The apparent resilience of some sponge species and the sensitivity of others highlight the need to understand the molecular basis of sponge responses to environmental stressors in order to determine if they will be able to adapt to rapidly changing ocean conditions. Future research focused on transcriptomic and metabolomic responses using genomic approaches will facilitate the assessment of molecular stress responses at different sponge life history stages.

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1© Springer International Publishing AG 2017
J.L. Carballo, J.J. Bell (eds.), Climate Change, Ocean Acidication and Sponges,
DOI10.1007/978-3-319-59008-0_1
Chapter 1
Climate Change andSponges: AnIntroduction
JoséLuisCarballo andJamesJ.Bell
Abstract This chapter provides an introduction to our current understanding of the
two most important features of climate change affecting marine sponges—ocean
warming and ocean acidication. Of these two stressors, thermal stress associated
with ocean warming is likely to have the greatest inuence on the sponge assem-
blages through the induction of diseases and mortality by a decrease in the efcacy
of defense mechanisms and development of pathogens. However, there is a consid-
erable variability among species in their responses to increasing temperature, and
some species have persisted during episodes of unusually high temperature.
Conspicuous sublethal effects have also been described. Thermal stress can limit
sponge reproductive capability and dispersal by causing the reabsorption of sper-
matic cysts and oocytes and by the disruption of the feedback mechanism that pre-
vents the release of asexual propagules when ecological factors are unsuitable for
propagule survival. Thermal stress also can affect sponge-feeding behavior by
increasing or decreasing ltration rates and by decreasing choanocyte chamber den-
sity and size, causing shifts in the microbial communities of the host sponge, and
can also increase the production of heat shock proteins, which leads to rapid upregu-
lation of genes involved in cellular damage repair. The effects of ocean acidication
on sponges are much less known, but recent studies have demonstrated the resis-
tance of certain species to lowered pH conditions. It seems that this capacity to
withstand OA lies in part in the ability of sponges to restructure their host- associated
microbiomes mainly by acquiring new microbial components via horizontal trans-
mission. The apparent resilience of some sponge species and the sensitivity of oth-
ers highlight the need to understand the molecular basis of sponge responses to
environmental stressors in order to determine if they will be able to adapt to rapidly
changing ocean conditions. Future research focused on transcriptomic and
J.L. Carballo (*)
Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México
(Unidad Académica Mazatlán), Avenida Joel Montes Camarena s/n,
PO Box 811, Mazatlán C.P.82000, Mexico
e-mail: jlcarballo@ola.icmyl.unam.mx
J.J. Bell
School of Biological Sciences, Victoria University of Wellington,
PO Box 600, Wellington, New Zealand
e-mail: James.bell@vuw.av.nz

2
metabolomic responses using genomic approaches will facilitate the assessment of
molecular stress responses at different sponge life history stages.
Keywords Sponges • Climate change • Thermal stress • Ocean acidication
1.1 The Two Main Climate Change Factors: Impact ofOW
andOA
Shifts in climate regimes are a recurrent feature of the Earth’s history (Zachos etal.
2001), but the peculiarity of modern-day changes is the unprecedented speed at
which they are occurring and the undeniable human inuence (Hansen etal. 2007),
in particular being driven by burning fossil fuels, cement production, and changes
in land use (IPCC 2007). These human activities are rapidly raising the atmospheric
carbon dioxide concentration (CO2) level at a rate that is unprecedented in at least
the last 22,000years (IPCC 2007; Joos and Spahni 2008).
It is predicted that by 2100, the CO2 concentration will be in the range of 541–
970ppm (IPCC 2001), and much of this anthropogenically generated CO2 will be
absorbed by the oceans. The increase in atmospheric carbon dioxide concentration
(CO2) will have two immediate consequences: (1) it will rise Earth’s atmospheric
temperature (global warming, GB) and, particularly, global sea surface tempera-
tures (SSTs) by up to 4°C (IPCC 2007), and (2) it will dissolve in seawater forming
carbonic acid (H2CO3), lowering the pH in a process known as ocean acidication
(OA). In the last 200years, the global ocean pH has dropped by 0.1 pH units (30%
increase in acidity), and it is predicted to drop a further 0.3–0.5units by 2100 (170%
increase in acidity), which is more than 100 times as rapid as at any time over the
past hundreds of the millennia (Meure etal. 2006).
Ocean warming and ocean acidication (pH, pCO2, and calcium carbonate satura-
tion) will impact marine organisms across all levels of biological organization, from
cellular to ecosystem levels. Ocean warming will affect marine benthic ecosystems
through epidemiologic diseases and mass mortalities of invertebrates, in particular
bivalves, corals, and sponges (Harvell etal. 2002; Webster 2007), and also cause coral
bleaching, species invasions, and shifts in species’ latitudinal ranges (Doney et al.
2012). Ocean acidication, in contrast, affects calcifying marine invertebrates most
severely, such as coralline algae (Kuffner etal. 2008), corals (Silverman etal. 2009),
echinoderms, and mollusks (Michaelidis etal. 2005). This is because it decreases the
availability of the carbonate ions required for skeletogenesis; abundanceof particular
group such as pteropod is expected to decline by half during this century due to
increased atmospheric carbon dioxide levels (Orr etal. 2005). OA and particularly
elevated CO2 also affect animals by disrupting the acid-base balance of internal uids,
leading to narcotizing acidosis, and also by triggering physiological mechanisms that
slow or stop metabolism (Knoll etal. 1996). Even more important, reductions in pH
may interfere with ion exchange, depressing metabolism and leading to a narrower
J.L. Carballo and J.J. Bell

3
window of thermal tolerance (Portner etal. 2005). Organisms that produce CaCO3
skeletons are particularly sensitive to hypercapnia, because carbonate biomineraliza-
tion requires precise control of the acid- base balance (Fabry etal. 2008).
1.2 Marine Sponges: AnIntroduction
Marine sponges are the evolutionary oldest multicellular animals that still exist,
with records from the Precambrian over 700 million years ago (Finks 1970), and a
large and consistent phylogenomic dataset supports sponges as the sister group to
all other animals (Simion etal. 2017).
Their long continued survival since then is closely linked to their simple level of
organization characterized by a lack of organs and true tissues and to the adaptabil-
ity of their body plan. In fact, they have been described as “dynamic multicellular
systems” whose cells have the ability to change into others if they need it, similar to
the stem cells in vertebrates (Bond 1992). This apparently simplistic body structure,
coupled with a unique tolerance to symbiotic microorganisms, gives sponges an
enormous versatility that greatly affects many aspects of their biology and allows
for a great diversity of evolutionary solutions for environmental challenges. In fact,
part of their evolutionary success is ascribed to their intricate association with a
diverse community of microorganisms that occur both intercellularly in the sponge
mesohyl and intracellularly (Thomas etal. 2016) and which can comprise 40–60%
of total tissue volume in some species (Taylor etal. 2007). For this reason, sponges
are described as “holobionts,” that is, a unit comprised of the sponge host and the
consortium of bacteria, archaea, unicellular algae, fungi, and viruses that reside
within it (Webster and Taylor 2012).
Sponges are widely distributed in marine systems and occur mainly in shallow
waters of the continental shelf, but there are species that can be found at 7000m
depth (Hooper and Van Soest 2002). Sponges represent a signicant component of
benthic communities in the oceans with respect to diversity, abundance, and their
potential to inuence benthic or pelagic processes. Thanks to their highly efcient
capability to pump water, over a half liter of water per second per kg dry mass (Weisz
etal. 2008), and the link they provide between nutrient transfer in the open water
column and the benthos, means they are important for benthic-pelagic coupling of
particulate and dissolved carbon (Gili and Coma 1998; Kahn and Leys 2016).
The relationship of sponges with macro- and microbial communities can also
facilitate high levels of benthic primary production and nutrient cycling, including
dissolved carbon (Mohamed etal. 2010; De Goeij et al. 2008), nitrogenous com-
pounds (Corredor et al. 1988; Jiménez and Ribes 2007), silicate (Reincke and
Barthel 1997; Maldonado etal. 2010), and phosphate (Zhang etal. 2015). Because
of this, sponges play a major role in the cycling of dissolved organic matter (DOM)
on coral reefs via the “sponge loop” pathway (de Goeij etal. 2013; Rix etal. 2017).
It has also recently been suggested that calcifying bacterial symbionts of sponges
may have been involved in the early evolution of the skeleton in the Precambrian
1 Climate Change andSponges: AnIntroduction

4
metazoans and represent a relict mechanism involved in the evolution of skeletons
in lower Metazoa bacteria-mediated skeletonization (Garate etal. 2017).
Sponges are also important habitat builders and can provide hard substrate and
add complexity in otherwise sediment-dominated environments, thereby increasing
abundance and biodiversity of the surrounding area (Dayton etal. 1974; McClintock
etal. 2005). Some species have essential functions in binding unconsolidated sub-
strate such as coral rubble and pebbles into stable surfaces (Wulff 1984). Sponges
are also important bioeroders in coral reefs, coralline bottoms, and oyster beds,
where they are able to excavate tunnels and galleries into calcium carbonate (Rützler
2002; Schönberg 2008; Carballo etal. 2013; Hernández-Ballesteros etal. 2013).
Because of their feeding habits, sponges can accumulate a wide range of pollut-
ants from both the suspension and dissolved phases, and they are considered useful
biomonitoring organisms and can provide convenient tools for characterizing the
state of a marine ecosystem (Carballo etal. 1996; Carballo and Naranjo 2002). They
are capable of accumulating metals (Zahn etal. 1981; Cebrian etal. 2006), organo-
chlorinated compounds (Pérez etal. 2003), radionuclides (Patel etal. 1985), and
combustion-derived PAHs in relation to petrogenic compounds (Batista etal. 2013).
Recently Theonella sp. has been shown to possess a specic and unique bacterial
system for element accumulation and mineralization of both arsenic and barium
(Keren etal. 2017).
1.3 Direct Impacts ofClimate Change onSponges
Unable to escape fromthe alteration of their environment, sponges are particularly
exposed to environmental factors, which control their survival, distribution, and
physiological performance. Thus, the changes associated with climate change will
have diverse consequences on sponge survival and tness. Research into the effects
of climate change on sponges initially focused on thermal sensitivities. Thus, the rst
study that associated a positive thermal anomaly with sponges was that by Vicente
(1989), who suggested that higher water temperature was responsible for the mortal-
ity and extinction of sponges of the genera Spongia and Hippospongia in the
Caribbean. No explanation of the causes of the mortality was given, but a decade
later, in 1999, a massive mortality, also of Spongia, Hippospongia, and Cacospongia,
coincided with a sudden increase in seawater temperature, higher than normal in the
Mediterranean Sea. In this case, it was hypothesized that the cause of that mortality
could be due to an extensive attack by opportunistic protozoans and fungi on the
sponges (Cerrano etal. 2000). Subsequent studies have attributed sponge mortality
to abnormal temperatures as a result of the loss of symbionts and the subsequent
establishment of alien microbial populations, including potential pathogens (Webster
etal. 2008; Cebrián etal. 2011). However, unusually high temperature does affect all
sponge species by the same way. For example, Chondrilla cf. nucula survived during
an episode of unusually high temperature that caused severe coral bleaching in the
Caribbean (Aronson etal. 2002). Furthermore, some encrusting boring sponges tend
J.L. Carballo and J.J. Bell

5
to spread faster into and over corals, increasing bioerosion and killing corals, during
high temperature events (Rützler 2002). Interestingly, some of these excavating
sponges harbor zooxanthellae in symbioses, which are much less affected by bleach-
ing than corals (Fang etal. 2016).
Unusual increases in temperature not only cause sponge mortality but also affect
physiological performance and reproductive capability and dispersal. Massaro etal.
(2012) showed a signicant reduction in ltration rate and lower choanocyte cham-
ber density and size in Rhopaloeides odorabile at only 2°C higher than the average
ambient seawater temperature. However, this response is not ubiquitous as other
species, such as Halichondria panicea, increased ltration rates at seawater tem-
peratures 5.5 °C above the normal ambient temperature (Riisgard et al. 1993).
Further studies of thermal stress and sponge-feeding ecology are necessary for
determining the mechanisms for this selective behavior. Water temperatures may
have important implications for population reproductive success where oogenesis
and spermatogenesis and larval release are cued by minimum and maximum water
temperatures (Ettinger-Epstein etal. 2007). Thus, thermal stress has been also asso-
ciated with the reabsorption of spermatic cysts and oocytes in the sponge Petrosia
sp. (Asa etal. 2000) and to the disruption of the feedback mechanism that prevents
the release of propagules of C. reniformis when ecological factors do not favor their
survival (Sugni etal. 2014). Surprisingly, Rhopaloeides odorabile larvae are remark-
ably able to withstand seawater temperatures up to 9 °C above normal, despite
adults being susceptible (Webster etal. 2013).
It is important to also mention that unusually low seawater temperatures have
also been associated with the mortality of sponges in temperate latitudes (Pérez
etal. 2006) and to sublethal effects, such as slowing growth and causing contraction
in size of some species (Fowler and Laffoley 1993).
On the other hand, not much is known about the effect of thermal stress on deep
sea sponge populations, despite that mass mortalities of important deep-water popu-
lations of Geodia barrette were associated to an unusual increase of water tempera-
ture in a cold-water coral reef (Norwegian shelf) (Guihen etal. 2012). However,
later studies determined that G. barrette has a high thermal tolerance, and a highly
stable microbiome even at temperatures 5°C above ambient, and that other ecologi-
cal processes such as low oxygen concentrations, elevated nutrients levels and
reduced salinity should be explored to provide insight into the cause:effect path-
ways of G. barrette mortality (Strand etal. 2017). The apparent resilience of some
sponge species and the sensitivity of others highlight the need to understand the
molecular basis of sponge responses to environmental stressors and to understand if
they may be able to adapt to rapidly changing ocean conditions. This was investi-
gated for the rst time in the sponge Suberites domuncula, which expressed a poly-
peptide after heat treatment (Bachinski etal. 1997). Higher-than-normal temperatures
also caused a signicant increase in heat shock protein Hsp70 transcript levels in the
Caribbean sponge Xestospongia muta (López-Legentil etal. 2008) and in Hsp40
and Hsp90 in Rhopaloeides odorabile, indicating the activation of a heat shock
response system. Exposure to high temperatures also produces a rapid downregula-
tion of many genes (actin-related protein, ferritin, calmodulin) and the induction of
1 Climate Change andSponges: AnIntroduction

6
others involved in signal transduction and in the innate immunity pathways, which
affects expression patterns of genes involved in cellular damage repair, apoptosis,
signaling, and transcription (Pantile and Webster 2011). It is likely that differences
in ecological and physiological features of different sponges, and even their differ-
ent life stages, will reect variations in thermal tolerance and resilience. Haliclona
tubifera subjected to elevated temperature showed activation of various processes
that interact to maintain cellular homeostasis. It seems that this species, which is
normally located in shallow water, is exposed to variable temperatures and has a
more robust response to temperature uctuations compared to sponges found at
deeper depths with colder and more stable temperatures (Guzmán and Conaco
2016).
Regarding OA, it has been shown that acidication decreases the diversity, bio-
mass, and trophic complexity of benthic communities (Kroeker etal. 2013). However,
both experimentally (Duckworth etal. 2012) and through eld research of sponges
across natural temperatures and pH ranges, such as those occurring in naturally acidi-
ed areas close to CO2 seeps, have been demonstratedthe resistance of certain sponges
to low-pH conditions (Morrow etal. 2015). It seems that their capacity to withstand
OA lies in their ability to restructure their host-associated microbiomes mainly by
acquiring new microbial components via horizontal transmission (Goodwin et al.
2014). Species with greater microbial diversity may develop functional redundancy
that could enable the holobiont to survive even if particular microbes are lost at low-
pH conditions (Ribes etal. 2016). It has also been suggested that OA may provide a
potential advantage for boring sponges, since OA accelerates bioerosion (Duckworth
and Peterson 2013; Wisshak etal. 2014). Recent research has demonstrated increased
bioerosion rates under experimentally elevated partial pressures of seawater carbon
dioxide (pCO2) with or without increased temperatures, which may lead to net erosion
on coral reefs in the future (Wisshak etal. 2012). However, this may depend on the
ability of sponges to survive and grow in the warmer and more acidic future environ-
ments and, fundamentally, on the energy reserves they have accumulated through the
rest of the year (Fang etal. 2014). It is important to note that there has been relatively
little research investigating about how ocean acidication affects the interaction
between coral and boring sponges, which is important as OA weakens and chemically
dissolves the coral skeletons, making boring easier (Stubler etal. 2014). As seawater
pH decreases, many corals are likely unable to create new layers of calcium carbonate
as efciently resulting in net erosion rates on reefs.
More information of the potential effect of OA on sponges comes from the past.
The overturning of anoxic deep oceans during the Permian-Triassic boundary
occurred about 252 million years ago and introduced high concentrations of carbon
dioxide into surface environments (Knoll etal. 1996), which is thought to be respon-
sible for the extinction of marine organisms that produced calcareous hard parts,
notably reef-building calcareous sponges (Knoll etal. 1996; Pörtner etal. 2004;
Pruss and Bottjer 2005), but also the majority of siliceous sponge species (88–92%),
including all hexactinellids and species with tetraxons (Liu etal. 2008). Low meta-
bolic rate, the absence of a circulatory system, and gas-permeable surfaces may
increase vulnerability in siliceous sponges (Knoll etal. 1996).
J.L. Carballo and J.J. Bell

7
Most studies concerning the impact of climate change on sponges discuss inde-
pendent effects of warming and ocean acidication, but it is also necessary to
include synergies with other local effects, such as pollution, sedimentation, and
other anthropogenic stressors. Understanding the connection between the different
local effects and climate-related stressors will be also necessary in order to predict
the consequences of future climate change on the survival of sponge populations. It
is also important to predict the biological stress responses of sponges to climate
change and ocean acidication in order to understand how sponges can modify their
gene expression as a potential mechanism for surviving in the future.
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