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Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean


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Global warming and increased atmospheric co 2 are causing the oceans to warm, decrease in pH and become hypercapnic. These stressors have deleterious impacts on marine inver-tebrates. Increasing temperature has a pervasive stimulatory effect on metabolism until lethal levels are reached, whereas hypercapnia has a narcotic effect. ocean acidification is a major threat to cal-cifying larvae because it decreases availability of the carbonate ions required for skeletogenesis and also exerts a direct pH effect on physiology. Marine invertebrate propagules live in a multistressor world and climate change stressors are adding to the mix. ocean pH, pco 2 and caco 3 covary and will change simultaneously with temperature, challenging our ability to predict future outcomes for marine biota. To address questions of future vulnerabilities, data on the thermo-and pH/pco 2 tolerance of fertilization and development in marine invertebrates are reviewed in the context of the change in the oceans that are forecast to occur over the next 100–200 years. Gametes and fertilization in many invertebrates exhibit a broad tolerance to warming and acidification beyond stressor values projected for 2100. Available data show that all development stages are highly sensitive to warming. larvae may be particularly sensitive to acidification/hypercapnia. Embryos that develop through the bottleneck of mortality due to warming may succumb as larvae to acidification. Early juveniles may be vulnerable to skeletal dissolution, although warming may diminish the negative impact of acidifi-cation on calcification. The effects of climate change stressors and their interaction differ among life history stages and species. Multistressor experiments show that if thermal thresholds are breached, embryos may not reach the calcifying stage. If the bottleneck for species persistence is embryonic thermotolerance, then the question of compromised calicification due to acidification may not be relevant. our limited knowledge of the interactive effects of climate change stressors is a major knowledge gap. Although climate change is deleterious for development in a broad range of marine invertebrates, some species and regional faunas will be more resilient than others. This has implica-tions for persistence, faunal shifts, species invasions and community function in a changing ocean.
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Oceanography and Marine Biology: An Annual Review, 2011, 49, 1–42
© R. N. Gibson, R. J. A. Atkinson, J. D. M. Gordon, I. P. Smith and D. J. Hughes, Editors
Taylor & Francis
Schools of Medical and Biological Sciences, University of Sydney, Australia
Abstract Global warming and increased atmospheric CO2 are causing the oceans to warm,
decrease in pH and become hypercapnic. These stressors have deleterious impacts on marine inver-
tebrates. Increasing temperature has a pervasive stimulatory effect on metabolism until lethal levels
are reached, whereas hypercapnia has a narcotic effect. Ocean acidication is a major threat to cal-
cifying larvae because it decreases availability of the carbonate ions required for skeletogenesis and
also exerts a direct pH effect on physiology. Marine invertebrate propagules live in a multistressor
world and climate change stressors are adding to the mix. Ocean pH, pCO2 and CaCO3 covary and
will change simultaneously with temperature, challenging our ability to predict future outcomes
for marine biota. To address questions of future vulnerabilities, data on the thermo- and pH/pCO2
tolerance of fertilization and development in marine invertebrates are reviewed in the context of the
change in the oceans that are forecast to occur over the next 100–200 years. Gametes and fertilization
in many invertebrates exhibit a broad tolerance to warming and acidication beyond stressor values
projected for 2100. Available data show that all development stages are highly sensitive to warming.
Larvae may be particularly sensitive to acidication/hypercapnia. Embryos that develop through the
bottleneck of mortality due to warming may succumb as larvae to acidication. Early juveniles may
be vulnerable to skeletal dissolution, although warming may diminish the negative impact of acidi-
cation on calcication. The effects of climate change stressors and their interaction differ among life
history stages and species. Multistressor experiments show that if thermal thresholds are breached,
embryos may not reach the calcifying stage. If the bottleneck for species persistence is embryonic
thermotolerance, then the question of compromised calicication due to acidication may not be
relevant. Our limited knowledge of the interactive effects of climate change stressors is a major
knowledge gap. Although climate change is deleterious for development in a broad range of marine
invertebrates, some species and regional faunas will be more resilient than others. This has implica-
tions for persistence, faunal shifts, species invasions and community function in a changing ocean.
As the planet warms due increased atmospheric CO2, so does the ocean. Direct uptake of CO2
is also causing ocean acidication, physiological hypercapnia and reduced carbonate saturation
(Caldiera & Wickett 2003, Feely et al. 2004, 2009, Orr et al. 2005, Intergovernmental Panel on
Climate Change [IPCC] 2007). Temperature, pH, pCO2 and calcium carbonate (CaCO3) satura-
tion are among the most important environmental factors controlling the distribution, physiological
performance, morphology and behaviour of marine invertebrates (Kinne 1970, Pörtner et al. 2005,
Pörtner & Knust 2007, Pörtner 2008, Widdicombe & Spicer 2008, Doney et al. 2009). Climate
change is thus causing alterations to marine ecosystems with impacts that are evident from polar
to tropical regions (Harley et al. 2006, Hoegh-Guldberg et al. 2007, IPCC 2007, Poloczanska et al.
2007, Przeslawski et al. 2008, Brierley & Kingsford 2009, Mueter & Litzow 2009). Ocean warm-
ing is implicated in mass mortality, increased disease, hypoxia, coral bleaching, species invasions,
phenological shifts in planktonic food web dynamics, physiological limitation in oxygen delivery
and increased costs of metabolism (Southward et al. 1995, Stachowicz et al. 2002, Edwards &
Richardson 2004, Hoegh-Guldberg et al. 2007, Lester et al. 2007, O’Connor et al. 2007, 2009,
Pörtner & Knust 2007, Richardson 2008, Smale & Barnes 2008, Coma et al. 2009, Ling et al.
2009, Montes-Hugo et al. 2009, Travers et al. 2009, Compton et al. 2010, Hofmann & Todgham
2010, Pörtner 2010). Ocean acidication is a major threat to calcifying marine invertebrates because
it decreases the availability of the carbonate ions required for skeletogenesis, and it exerts a direct
pH effect. Hypercapnia has a pervasive narcotic effect suppressing metabolism (Pörtner et al. 2004,
Pörtner & Langenbuch 2005, Fabry et al. 2008, Pörtner 2008, Widdicome & Spicer 2008, Doney
et al. 2009, Melzner et al. 2009, Christensen et al. 2011).
Ocean pH, pCO2 and CaCO3 saturation covary and are changing simultaneously with ocean
temperature, challenging our ability to predict future outcomes for marine invertebrates in a chang-
ing ocean. Marine propagules live in a multistressor world, and the interactive effects of climate
change and other stressors are poorly understood (Harley et al. 2006, Pörtner 2008, Przeslawski
et al. 2008). Early life history stages are of particular concern because sensitivity to these stressors
may be the bottleneck for species persistence and ecological success in a changing ocean. For ben-
thic organisms, compromised performance of developmental stages has negative consequent effects
for adult populations and marine communities (Harley et al. 2006, Przeslawski et al. 2008, Brierley
& Kingsford 2009, Uthicke et al. 2009).
Many marine invertebrates broadcast-spawn their gametes for external fertilization and have
pelagic larvae that spend days to months in the water column (Figures 1, 2 and 3). Due to their sensi-
tivity to water chemistry marine gametes and embryos have long been used as a bioassay system for
monitoring of environmental pollutants (Dinnel et al. 1987, Ringwood 1992, Carr et al. 2006, Byrne
et al. 2008). As the impacts of anthropogenic pressures on the marine environment became evident
in the twentieth century, a plethora of ecotoxicological studies documented the response of devel-
opmental stages to pollutants including ocean warming (e.g., power plant efuent) and acidication
(e.g., acid leachates, porewater) (e.g., Greenwood & Bennett 1981, Bay et al. 1993, Riveros et al.
1996, Schiel et al. 2004, Carr et al. 2006, Byrne et al. 2008). Recognition of the impact of climate
change on the marine environment has generated a new focus on these stressors in order to under-
stand how marine species will respond to ocean change. In contrast to point source pollution, the
oceans are experiencing long-term pervasive perturbation due to increased warming and CO2 upta ke
that has taken place since the Industrial Revolution (Caldiera & Wickett 2003, Zeebe et al. 2008).
The ‘business-as-usual’ scenario for global change (A1F1, IPCC 2007) provides a framework
with which to assess comparative vulnerabilities of species and their life history stages. Although
there is uncertainty with regard to levels of change, an increase in ocean pCO2 from present levels
of about 380 ppm to 700–1000 ppm by 2100 and 2000 ppm by 2300 can be expected (Caldiera
& Wickett 2005, IPCC 2007, Doney et al. 2009). This increase is projected to result in a drop in
surface ocean pH by 0.14–0.41 units and 0.30–0.7 units, respectively, over the same timescale.
Increasing temperature is the most pervasive of present-day impact of climate change on marine
systems (Poloczanska et al. 2007, Halpern et al. 2008, Brierley & Kingsford 2009). The estimate
for increase in mean sea-surface temperatures (SSTs) by 2100 is predicted to lie between 1.1 and
6.4°C with the best estimates ranging between 2 and 4.5°C (IPCC 2007). These are consensus pro-
jections, and the magnitude of change is differing markedly between regions (IPCC 2007, Brierley
& Kingsford 2009). Regional differences in the extent of ocean warming highlight the need for a
regional approach in assessment of ecosystem change and risk to species. The potential impacts
of ocean change on marine invertebrate reproduction and development need to be considered in a
regional, seasonal, depth- and habitat-relevant context. For instance, cold high-latitude waters are the
rst to become carbonate undersaturated, so ocean acidication is a serious contemporary stressor
for polar species, as seen in decalcied Arctic pteropods and poorly calcied Antarctic Foraminifera
(Orr et al. 2005, Comeau et al. 2009, Fabry et al. 2009, McClintock et al. 2009, Moy et al. 2009).
Ocean warming is the most serious immediate climate change stressor for some regions, including
the Mediterranean, southern North Sea, Western Antarctic Peninsula and south-eastern Australia
(Ridgway 2007, Barnes & Peck 2008, Coma et al. 2009, Richardson et al. 2009, Schmalenbach &
Franke 2010, Schoeld et al. 2010). Seasonal change is also a consideration as evidenced by dispro-
portionate wintertime ocean warming in south-eastern Australia and the North Sea, with expected
greater impacts for winter spawners and planktonic phases (Poloczanska et al. 2007, Schmalenbach
& Franke 2010), and the greater wintertime decrease in CaCO3 saturation in the Southern Ocean,
with aragonite undersaturation projected to occur in winter by 2030 (McNeil & Matear 2008) and
year round by 2050 (Orr et al. 2005).
To date most studies on the impacts of climate change on invertebrate development have focused
on ocean acidication as a sole stressor (reviews: Doney et al. 2009, Byrne 2010, Dupont et al.
2010a, Hendriks et al. 2010a, Kroeker et al. 2010), with some studies on the effects of ocean warm-
ing (e.g., Negri et al. 2007, Whalan et al. 2008, Byrne et al. 2011a). A few studies have investigated
the interactive effects of warming and CO2-driven acidication on marine life histories (Findlay
Fertilized embryo
Advanced brachiolaria
Bipinnaria Brachiolaria
Figure 1 Life cycle of the seastar Patiriella regularis. For ecological success all life stages have to be com-
pleted. Different life stages will have differing sensitivities to climate change stressors. (Photographs from
Byrne & Barker 1991 with permission.)
et al. 2008, 2010a,b, Byrne et al. 2009, 2011b, Parker et al. 2010, Sheppard Brennand et al. 2010).
Development can fail at any stage, and determination of the comparative sensitivities of planktonic
(e.g., gametes, fertilization, embryos, larvae) and benthic (juveniles, adults) life stages to climate
change stressors is needed to identify vulnerabilities. Successful recruitment and persistence of
populations require that all ontogenetic stages be completed successfully (Figure 1).
In this review, data on the thermo- and pH/pCO2 tolerance of marine invertebrate gametes and
developmental stages are assessed within the context of ocean change in the near future. The data
are largely from single-stressor physiology, ecotoxicology and global change studies. For ocean
acidication, only CO2-driven acidication is considered. The impacts of acidication generated by
use of mineral acid are reported elsewhere (Albright et al. 2008, Fabry et al. 2008, Kurihara 2008,
Byrne 2010, Dupont et al. 2010a). Impacts of ocean warming and acidication on environmental
control of reproduction (fecundity, maturation, spawning) and on adult physiology are documented
in several reviews (Somero 2002, Przeslawski et al. 2005, 2008, Melzner et al. 2009). Identication
of the marine invertebrate life history stages that are most vulnerable to climate change is needed
to determine bottlenecks for species persistence in a changing ocean. Here, data on the impacts of
ocean warming and acidication are used to address questions of stage-specic vulnerabilities in
development and the potential resilience of marine invertebrates in a changing ocean. The focus is
on the impact of warming and acidication on development from fertilization to the benthic juvenile
with inclusion of key insights from studies of the adult stage.
Impacts of ocean warming and acidication
on fertilization in marine invertebrates
Although the fertilization biology of marine invertebrates is highly sensitive to water chemistry
and deleterious effects have been documented for a plethora of anthropogenic stressors (e.g., trace
metals, acid leachates, porewater, efuents) (e.g., Riveros et al. 1996, Carr et al. 2006, Byrne et al.
2008), the weight of evidence from diverse species indicates that fertilization in many species is
robust to near-future ocean warming, acidication and hypercapnia (Table 1, Figure 2). The effects
of increased acidication/hypercapnia and warming on fertilization are best documented for shal-
low water and intertidal species, many of which have been used as model organisms for laboratory
studies (Table 1).
Thermotolerance of fertilization
Single-stressor studies show that broadcast spawners (ca. 5 corals, 2 polychaetes, 4 molluscs,
16 echinoderms) achieve high rates of fertilization over a wide temperature range (Table 1, Figure 2)
and at warming levels well beyond those projected for extreme ocean change. It appears that near-
future upper warming scenarios of about 4–6°C would not impair fertilization in the species listed
in Table 1.
Increased temperature and the associated decrease in seawater viscosity increase fertilization
success due to stimulation of sperm metabolism, facilitation of the acrosome reaction and increased
sperm swimming speed (Mita et al. 1984, Lewis et al. 2002, Kupriyanova & Havenhand 2005). The
thermal robustness of fertilization may be due to the presence of maternal factors (e.g., heat shock
proteins) that protect early embryos (prior to onset of zygotic gene expression) against environmen-
tal stressors and the temperature-independent period in early development (Yamada & Mihashi
1998, Hamdoun & Epel 2007). This protection may be enhanced in species with large eggs and
lecithotrophic development for which the evolutionary (heterochronic) switch to loading of maternal
transcripts into eggs facilitates rapid development (Raff & Byrne 2006). For oysters, elevated tem-
perature over an 8°C range (18–26°C) resulted in increased fertilization at higher temperature but a
decrease if the temperature increase exceeded 12°C (30°C) (Parker et al. 2010). The robust nature
Table 1 Inuence of increased temperature (°C) and acidication (pH/pCO2, ppm) as single
stressors on fertilization in marine invertebrates and levels for signicant deleterious effects
in the context of near-future ocean change (100–200 years)
Phylum, species
Temperature Acidication (pH/pCO2)
Range for
fertilization of
75% or more
increase above
local ambient
for fertilization
pH range for
fertilization of
75% or more
pH at which
is reduced to
Acropora millepora 28–31 4 ND ND Negri et al. 2007
Diploria strigosa 30–32 >4 ND ND Bassim et al. 2002
Favites abdita 26–32 >5 ND ND Negri et al. 2007
Favites chinensis 26–32 >5 ND ND Negri et al. 2007
Mycedium elephantotus 26–32 >5 ND ND Negri et al. 2007
Parborlasia corrugatus 0–1 ND 7.0–8.0
528–5806 ND Ericson et al. 2010
Galeolaria caespitosa 21 5 ND ND Kupriyanova &
Havenhand 2005
Nereis virens 10–18 15 ND ND Lewis et al. 2002
Haliotis coccoradiata 20–24 ND 7.6–8.2
ND Byrne et al. 2010b
Crassostrea gigas 18–30 ND 7.4–8.2
ND Kurihara et al.
2007, Kurihara
2008, Havenhand
& Schlegal 2009
18–30 ND 7.9–8.2
Parker et al. 2010
Mytilus galloprovincialis 13 ND 7.4–8.0
ND Kurihara 2008
Saccostrea glomerata 26 >4 8.0–8.2
Parker et al. 2010
Spisula solidissima 8–20 >10 ND ND Clotteau & Dubé
Acanthaster planci 28–31 6 ND ND Rupp 1973
Asterias amurensis 10–20 12 ND ND Lee et al. 2004
Culcita novaeguineae 28–34 8 ND ND Rupp 1973
Linckia laevigata 28–34 8 ND ND Rupp 1973
(continued on next page)
Table 1 (continued) Inuence of increased temperature (°C) and acidication (pH/pCO2, ppm)
as single stressors on fertilization in marine invertebrates and levels for signicant deleterious
effects in the context of near-future ocean change (100–200 years)
Phylum, species
Temperature Acidication (pH/pCO2)
Range for
fertilization of
75% or more
increase above
local ambient
for fertilization
pH range for
fertilization of
75% or more
pH at which
is reduced to
Patiriella regularis 20–26 ND 7.6–8.2
ND Byrne et al. 2010b
Meridiastra calcar 18–23 ND 7.6–8.2
ND Nguyen, H. pers.
Anthocidaris crassispina 15–30 ND ND ND Mita et al. 1984
Arbacia punctulata ND ND 7.0–8.6 <7.0 Carr et al. 2006
Centrostephanus rodgersii 18–24 ND 7.6–8.2
ND Byrne et al. 2010b
Dendraster excentricus 7–26 13 ND ND Bingham et al.
Diadema savignyi 28–36 >8 ND ND Rupp 1973
Echinometra lucunter 15–36 9 ND ND Sewell & Young
Echinometra mathaei 28–36 8 7.7–8.1
Rupp 1973,
Kurihara &
Shirayama 2004
Heliocidaris erythrogramma 17–26 ND 7.6–8.2
ND Byrne et al. 2009,
2010a,b, 2011a,b
Heliocidaris tuberculata 17–24 ND 7.6–8.2
ND O’Connor &
Mulley 1977,
Byrne et al.
Hemicentrotus pulcherrimus 0–30 15 7.4–8.0
Mita et al. 1984,
Fujisawa 1995,
Kurihara &
Shirayama 2004
Parechinus angulosus 15–19 8 ND ND Greenwood &
Bennett 1981
Sterechinus neumayeri 0–1 ND 7.7–8.0
Ericson et al. 2010
Strongylocentrotus purpuratus ND ND 7.3–8.2 7.2 Bay et al. 1993
Tripneustes gratilla 20–27 ND 7.6–8.2
ND Rahman et al.
2009, Byrne
et al. 2010b
Note: The temperature data are impacts of thermal increase at ambient pH. The pH data are the response to acidication at
the control/optimal temperature used for fertilization. Experimental pH was adjusted by treatment of seawater with
CO2 gas. Where temperature range was not investigated, ambient/control values were determined from the study. ND,
no data
a At low sperm concentration.
of marine invertebrate gametes and fertilization to warming is reected in routine use of heat shock
(ca. 10°C above ambient) to obtain fertile gametes for developmental studies and aquaculture (e.g.,
Selvakumaraswamy & Byrne 2000, Ramofaa et al. 2003, Parker et al. 2009).
pH/pCO2 tolerance of fertilization
Hypercapnia narcotizes sperm and is used in vivo to maintain sperm in a quiescent state and pre-
serve energy stores (Chia & Bickell 1983, Johnson et al. 1983, Ward et al. 1985, Brokaw 1990). The
Heliocidaris tuberculata
Tripneustes gratillaCentrostephanus rodgersii
Haliotis coccoradiata Patiriella regularis
% Fertilization
pH 8.2
327–335 814–851 1051–1104 1729–1828 327–335 1051–1104 1729–1828
7.9 7.8 7.6 8.2 7.8 7.6
Heliocidaris erythrogramma
Figure 2 Percentage of fertilization in the echinoids Heliocidaris tuberculata, H. erythrogramma,
Tripneustes gratilla and Centrostephanus rodgersii, the asteroid Patiriella regularis and the abalone Haliotis
coccoradiata in response to ambient and projected ocean change scenarios for year 2100 (A1F1, IPCC 2007).
Experiments in the left panel used four pH and three temperature levels, while those in the right panel used
three pH and three temperature levels. Experimental temperatures varied due to seasonal differences in the
timing of gamete maturation in the different species. pCO2 levels are indicated for each pH used. Error bars
are 95% condence intervals. (From Byrne et al. 2010a, with permission.)
mechanisms underlying the effects of hypercapnia on sperm are well understood and involve control
of intracellular pH (pHi) by CO2. Hypercapnia reduces sperm swimming speed, so it is suggested
that ocean acidication may impair fertilization (Havenhand et al. 2008, Morita et al. 2010). In
nature, however, release of sperm into the water column overcomes hypercapnic effects due to the
respiratory dilution effects (increased oxygen tension) of seawater (Chia & Bickell 1983). This is not
the case for a sea cucumber and a coral (Morita et al. 2006, 2009). Egg-derived compounds promote
sperm motility at low pH, a response reported for many species of corals, molluscs, echinoderms and
ascidians and is triggered by a cGMP (cyclic guanosine monophosphate) cascade (Miller 1985, 1997,
Ward et al. 1985, Bolton & Havenhand 1996, Riffell et al. 2002, Morita et al. 2006, 2009, Darszon
et al. 2008). Asteroid egg jelly facilitates the acrosome reaction by increasing the pHi of sperm
(Matsui et al. 1986). Where the compounds have been characterized, they are usually egg jelly pep-
tides (Morita et al. 2006, 2009, Darszon et al. 2008). The robust nature of echinoderm eggs to acid
conditions is reected in the routine use of low pH (pH 5.0) to strip the jelly coat prior to fertilization
in functional studies of fertilization and this extracellular layer (e.g., Johnson & Epel 1975).
Despite potential narcotic effects of hypercapnia on sperm swimming, many single-stressor
studies (ca. 1 coral, 1 nemertean, 4 molluscs, 10 echinoderms) indicated that fertilization in diverse
species is robust to pH 7.4–7.6 (pCO2 1000 ppm), pH levels driven by CO2 uptake well below
acidication projected for surface ocean waters by 2100 (Table 1, Figure 2). The resilience of fer-
tilization of the species in Table 1, many of which are intertidal and shallow subtidal species, may
reect adaptation to the uctuating pH and hypercapnic conditions in their habitat. In those studies
in which far-future acidication scenarios were considered, deleterious effects on fertilization were
reported at pH 7.4 and less (Table 1).
Although data are limited, there are inferences that sensitivity of fertilization to acidica-
tion may differ among species from differing habitats. In the intertidal sea urchin Heliocidaris
erythrogramma fertilization is robust to low pH (pH 7.6) even at very low sperm concentrations
(10 sperm to 1 egg, 10 sperm ml−1) (Byrne et al. 2009, 2010a,b, but see Havenhand et al. 2008). By
contrast, fertilization in its subtidal congener H. tuberculata appears to be more sensitive to near-
future ocean acidication (Byrne et al. 2010a). A fertilization kinetics study of the subtidal species
Strongylocentrotus franciscanus showed that acidication (pH 7.55, pCO2 1800 ppm) shifted the
fertilization curve to a lower success rate (Reuter et al. 2011). By contrast fertilization was only
impaired at pH 7.4 at low sperm concentrations (50 sperm to 1 egg) in the subtidal Antarctic spe-
cies Sterechinus neumayeri (Ericson et al. 2010). In studies of the coral Acropora palmata where
controls were 50% of fertilization, fertilization was reduced by ca. 60% (i.e., 30% fertilization) at
pH 7.7/pCO2 998 (Albright et al. 2010).
Conicting results on the effects of decreased pH on fertilization have been obtained for the
same species, for example in echinoids (Havenhand et al. 2008, Byrne et al. 2009) and oysters
(Kurihara et al. 2007, Havenhand & Schlegal 2009, Parker et al. 2010). In a recent study of the oys-
ter Crossostrea gigas a decrease in fertilization success was recorded at pH 7.8 (Parker et al. 2010),
but this was not observed in previous studies (Kurihara et al. 2007, Havenhand & Schlegal 2009)
even in extreme treatments (pH 7.4, pCO2 2268 ppm). For Heliocidaris erythrogramma a decrease
in fertilization at low pH (pH 7.7) was reported (Havenhand et al. 2008), but this was not conrmed
in subsequent studies (Figure 2).
Empirical data from a greater diversity of species from different habitats are needed to dis-
cern trends, with interstudy comparison facilitated by use of comparable experimental methods.
Differences in experimental conditions (e.g., gamete source, gamete age, sperm-egg contact time,
gamete concentration, test vessel volume, vessel type, stage scored) are well known to inuence
fertilization test results (Bay et al. 1993, Clotteau & Dubé 1993, Styan 1998, Palumbi 1999, Baker
& Tyler 2001, Evans & Marshall 2005, Lera et al. 2006, Byrne et al. 2010a,b), highlighting problems
with interstudy comparisons. For instance in various studies fertilization is arrested/reduced fol-
lowing treatments using a range of chemical agents (e.g., xatives, KCl, lauryl sulphate; e.g., Styan
et al. 2005, Carr et al. 2006, Reuter et al. 2010) or rinsing off excess sperm (e.g., Havenhand et al.
2008, Byrne et al. 2009), whereas other fertilization studies do not use these procedures (e.g., Evans
and Marshall 2005). The source of gametes used for experiments, either pooled from multiple males
and females to represent a population of spawners or in single dam-sire crosses as in fertilization
kinetics and quantitative genetics studies, is also a major source of interstudy variation due to the
strong genetic effect of male-by-female interactions (Evans & Marshall 2005, Levitan & Ferrell
2006, Evans et al. 2007). It is well known that variation in sperm quality and egg-sperm compat-
ibility determine fertility in echinoids and oysters (Palumbi 1999, Boudry et al. 2002). In addition,
some studies score fertilization based on the presence of a fertilization envelope, whereas others
used embryonic mitosis (cleavage). These are not equivalent stages and have different sensitivities
to stressors (see Byrne et al. 2009, Allen & Pechenik 2010).
Due to the plethora of factors inuencing variation in fertilization tests in interlaboratory com-
parisons (e.g., same species, same reference toxicant) for environmental monitoring (Bay et al. 1993,
Lera et al. 2006), standard test protocols have been established (e.g., Cherr et al. 1990, American
Society for Testing and Materials [ASTM] 2004). It is not clear if this standardization is warranted
for global change studies. It appears that fertilization may not be a suitable endpoint for assessing
the impacts of climate change stressors on marine life histories. Later developmental stages provide
better test endpoints with less conict among studies (Table 2).
Impacts of ocean warming and acidication
on marine embryos and larvae
With concerns about the impacts of climate change on marine biota, the impacts of ocean warm-
ing and acidication on development are being investigated in an increasing number of spe-
cies. Experimental approaches to rearing embryos and larvae in ocean change conditions vary
between studies. In studies investigating ocean acidication as a single stressor the most common
approach has involved transfer of developmental stages from contemporary seawater conditions
(e.g., hatchery-reared larvae, eld recruits) to decreased pH conditions (Kurihara & Shirayama 2004,
Findlay et al. 2008, 2010, Miller et al. 2009, Ries et al. 2009, Talmage & Gobler 2009, Albright et al.
2010, Beniash et al. 2010, Findlay et al. 2010a,b, Range et al. 2011). However, developmental success
requires that all ontogenetic stages are completed successfully (Figure 1), so the applicability of this
approach to climate change effects is not clear. The integrative and cumulative effects of stressors
across ontogenetic stages are likely to inuence experimental outcomes. Depending on species and
stressor type, early embryos and larvae exhibit different sensitivities to stressors in many studies
(Pechenik 1987, Ringwood 1992, Allen & Pechenik 2010, Ericson et al. 2010). A study comparing
the effects of ocean acidication on veliger larvae derived from embryos fertilized in both control
and experimental conditions found greater deleterious effects (lower survivorship, smaller larvae)
in larvae from the latter treatments (Parker et al. 2010). A similar difference was seen in asteroid
larvae (Foo 2010). There are insufcient data to determine if experimental outcomes differ with
respect to the developmental stage at which incubations are initiated. However, it is most realistic,
where possible, to assess the impact of climate change stressors from the outset of development in
embryos fertilized in experimental conditions. A few studies have taken this approach (e.g., Byrne
et al. 2009, 2010a, 2011b, Parker et al. 2010, Sheppard Brennand et al. 2010).
Most studies on the impacts of ocean change on development have focused on calcifying larval
stages due to concerns of reduced aragonite and calcite saturation (Table 2, Figures 3, 4 and 5).
In general there is only limited knowledge of effects of acidication on early stages (e.g., embry-
onic mitosis/cleavage, morulae, blastulae, gastrulae). More data are needed on developmental
Table 2 Inuence of increased temperature (°C) and acidication (pH/pCO2, ppm) as single stressors on embryonic and larval development in
marine invertebrates and levels for signicant deleterious effects in the context of near-future ocean change (100–200 years)
Phylum, species
Temperature Acidication (pH/pCO2)
Optimum range for
(ca. 75% normal or above)
Temperature increase
negative effects
(ca. less than 75% normal)
on development
pH range for
normal (ca.
75%) embryo
and larval
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Rhopaleoeides odorabile 22–28 22–28 10 10 ND ND Whalan et al. 2008
Acropora digitata 27 ND ND NS 7.3–8.0
Smaller polyps
Suwa et al. 2010
Reduced metamorphosis
Nakamura et al. 2011
Acropora millepora 26–30 ND 4 ND ND ND Negri et al. 2007
Acropora muricata 26–32 26–32 4 ND ND ND Baird et al. 2006
Acropora palmata 28–30 28–30 4 4 ND ND Randall & Szmant 2009a
Acropora tenuis 27 ND ND ND 7.3–8.0
Smaller polyps
Kurihara 2008, Suwa et al.
Diploria strigosa 30–31 30–31 2 2 ND ND Bassim et al. 2002
Favites abdita 26–32 ND >4 ND ND ND Negri et al. 2007
Favia faragum 28–31 28–30 4 3 ND ND Randall & Szmant 2009b
Mycedium elephantotus 26–32 ND >4 ND ND ND Negri et al. 2007
Stylophora pistillata 23–25 23–25 >4 >4 ND ND Putnam et al. 2008
Parborlasia corrugatus 0–1 ND ND ND 7.3–8.0
7.0/5806 Ericson et al. 2010
Haliotis coccoradiata 20–22 20 4 2–4 8.0–8.2
Abnormal development,
decreased larval calcication
Wong et al. 2010; Byrne et al.
2011, Figure 4
Littorina obtusata 15 ND ND ND ND 7.6/1093
Abnormal development,
decreased metamorphosis
Ellis et al. 2009
Strombus gigas 20–32 20–32 ND ND ND ND Davis 2000
Argopecten irradians ND ND ND ND 8.1/360 7.5–7.8/690–1630 Talmage & Gobler 2009
Crassostrea ariakensis 25 ND ND ND 7.8–8.1
ND Miller et al. 2009
Crassostrea gigas 18–30 18–30 ND ND 7.8–8.2
Decreased larval calcication
Kurihara et al. 2007, Kurihara
Abnormal development,
decreased larval calcication
Parker et al. 2010
Crassostrea virginica 20–30 20–30 ND ND 8.0–8.2
7.76–7.9/572–840 MacInnes & Calabrese 1979,
Wright et al. 1983, Miller
et al. 2009, Talmage & Gobler
7.5/3500 Beniash et al. 2010
Mercenaria mercenaria ND ND ND ND 8/360 7.5–7.8/640–1500 Talmage & Gobler 2009
Mytilus edulis 5–20 5–20 5 5 ND ND Brenko & Calabrese 1969
Mytilus galloprovincialis 13 ND ND ND 8.1/380 7.4/2000
Smaller larvae
Kurihara et al. 2008a
Pinctada margaritifera 25–30 25–30 7 7 ND ND Doroudi et al. 1999
Saccostrea glomerata 22–30 22–26 ND ND 7.9–8.2
Smaller larvae
Parker et al. 2010, Watson et al.
(continued on next page)
Table 2 (continued) Inuence of increased temperature (°C) and acidication (pH/pCO2, ppm) as single stressors on embryonic and larval
development in marine invertebrates and levels for signicant deleterious effects in the context of near-future ocean change (100–200 years)
Phylum, species
Temperature Acidication (pH/pCO2)
Optimum range for
(ca. 75% normal or above)
Temperature increase
negative effects
(ca. less than 75% normal)
on development
pH range for
normal (ca.
75%) embryo
and larval
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Sepia ofcianalis 17 ND ND ND 7.1–8.0
ND Gutowska et al. 2008, 2010a,b
Ophiothrix fragilis 14 ND ND ND 8.1 7.7–7.9
Smaller larvae
Dupont et al. 2008
Acanthaster planci 28–31 ND 6 ND ND ND Rupp 1973
Asterias amurensis 10–15 10–15 >12 >12 ND ND Lee et al. 2004
Asterias rubens 10–20 ND >5 ND ND ND Benitez-Villalobos et al. 2006
Crossaster papposus 12 ND ND ND 7.7–8.1
Faster growth
ND Dupont et al. 2010b
Culcita novaeguineae 28–31 ND 6 ND ND ND Rupp 1973
Linckia laevigata 28–31 ND 6 ND ND ND Rupp 1973
Marthasterias glacialis 15–20 ND >5 ND ND ND Benitez-Villalobos et al. 2006
Patiriella regularis 18–22 18–22 4 4 7.6–8.25
ND Byrne & Barker 1991,
Foo, 2010
Meridiastra calear 18–21 ND 5 ND Nguyen, H., pers. comm.
Anthocidaris crassispina 16–29 16–26 >4 >4 ND ND Fujisawa 1989
Arbacia punctulata ND ND ND ND 7.0–8.6 6.8–7.0 Carr et al. 2006
Centrostephanus rodgersii 18–22 18–22 6 ND 7.8–8.2
7.6–78/1695–1762 Foo 2010
Dendraster excentricus 7–20 ND 9 ND ND ND Fujisawa 1993, Bingham et al.
Diadema savignyi 28–31 ND 6 ND ND ND Rupp 1973
Echinometra lucunter 23–34 ND 8 >10 ND ND Sewell & Young 1999
Echinometra mathaei 28–34 ND 8 ND 7.8–8.0
Smaller larvae
Rupp 1973, Kurihara 2008
Evechinus chloroticus 15 ND ND ND 7.7–8.1
Smaller larvae
Clark et al. 2009
Heliocidaris erythrogramma 18–24 18–24 4–6 4–6 7.6–8.2
No effect on early development
Byrne et al. 2009, 2010a,b,
Impaired juvenile calcication
Byrne et al. 2011b
Decrease in gastrula & larvae
Havenhand et al. 2008
Heliocidaris tuberculata 19–24 ND 4 ND ND ND O’Connor & Mulley 1977
Hemicentrotus pulcherrimus 5–23 5–23 >6 6 7.8–8.0
Smaller larvae
Fujisawa 1989, 1995, Kurihara
& Shirayama 2004
Lytechinus variegatus 15–18 ND ND ND ND 540–970
Smaller larvae
O’Donnell et al. 2010
Pseudechinus huttoni 10–12 ND ND ND 7.7–8.1
Smaller larvae
Clark et al. 2009
Pseudocentrotus depressus 9–25 9–25 >4 >4 ND ND Fujisawa 1989
Sterechinus neumayeri 0.2–1.7 ND >1 ND 7.3–8.0
Abnormal blastulae
Stanwell-Smith & Peck 1998,
Ericson et al. 2010
Smaller larvae
Clark et al. 2009
Strongylocentrotus franciscanus 15–18 ND ND ND ND 7.85–7.95/540–970
Reduced gene expression
O’Donnell et al. 2009
Strongylocentrotus purpuratus 5–16 ND ND ND 7.3–8.2 <7.2
Increased mortality
Bay et al. 1993, Fujisawa 1993
(continued on next page)
Table 2 (continued) Inuence of increased temperature (°C) and acidication (pH/pCO2, ppm) as single stressors on embryonic and larval
development in marine invertebrates and levels for signicant deleterious effects in the context of near-future ocean change (100–200 years)
Phylum, species
Temperature Acidication (pH/pCO2)
Optimum range for
(ca. 75% normal or above)
Temperature increase
negative effects
(ca. less than 75% normal)
on development
pH range for
normal (ca.
75%) embryo
and larval
Low pH/ pCO2 effects on
embryos, larvae or juvenilesEmbryos Larvae Embryos Larvae
Tripneustes gratilla 16–29 19–31 4 6 7.8–8.25
Smaller larvae
Clark et al. 2009, Rahman et al.
2009, Sheppard Brennand
et al. 2010
Acartia erythraea 27 ND ND ND 7.3–8.2
Increased mortality
Kurihara et al. 2004
Acartia tsuensis 25 ND ND ND 7.3–8.2
ND Kurihara & Ishimatsu 2008
Amphibalanus amphitrite 25–28 ND ND ND 7.4–8.2 7.4
No effect on larvae, smaller
McDonald et al. 2009
Calanus nmarchicus 8.8 ND ND ND 6.95–8.23
ND Mayor et al. 2007
Echinogammarus marinus 15 ND ND ND 7.5–8.0
ND Egilsdottir et al. 2009
Hommarus gammarus 19 ND ND ND 8.4/315 8.1/1202
No effect on early development,
less-calcied terminal larvae
Arnold et al. 2009
Palaemon pacicus 25 ND ND ND 7.9–8.2
Smaller juveniles, lower survival
Kurihara et al. 2008b
Note: The temperature data are the impacts of thermal increase at ambient pH. The pH data are the response to acidication at the control/optimal rearing temperature. Experimental pH
was adjusted by treatment of seawater with CO2 gas. Thermal limits are represented as increase (°C) above ambient. Where temperature range was not investigated, ambient/control
values were obtained from the study. ND, no data.
thermo- and pH tolerance for diverse species from the outset of development (fertilization) and
across ontogenetic stages. In particular, good comparative data for species from temperature
and pH-variable (e.g., intertidal, temperate) and temperature and pH-stable (e.g., subtidal, polar)
regions are needed. There is considerable variation among species in developmental sensitivity to
climate change stressors (Byrne 2010, Dupont et al. 2010a, Kroeker et al. 2010), and where possible,
research should involve closely related species to reduce experimental variation due to disparate
phylogeny (Sokolova & Pörtner 2001, Raff & Byrne 2006).
Figure 3 The life histories of benthic marine calciers include species with non-calcifying (A–D, J–N) and
calcifying (E–I) larvae. (A) Coral planula. (B) Reniera sp. sponge larvae. (C) Filograna implexa, polychaete
trochophore. (D) and (E) Haliotis spp. mollusc trochophore and veliger shell. (F) Siphonaria sp., mollusc
veliger larva. (G)–(I) Heliocidaris tuberculata, Centrostephanus rodgersii and Ophiactis resiliens, echin-
oderm plutei. (J) and (K) Patiriella regularis, asteroid bipinnaria and brachiolaria larvae. (L) Holothuria
scabra, holothuroid auricularia. (M) Cryptasterina pentagona, lecithotrophic brachiolaria. (N) Heliocidaris
erythrogramma, reduced pluteus. (O) crab zoea larva. (P) Nerita atramentosa and calcareous egg capsules.
(Q) Heliocidaris erythrogramma juvenile. (R) Parvulastra exigua juvenile. (Photographs courtesy of R.
Babcock (A), B. Degnan (B,C), E. Wong (D), L. Page (E,F,P), I. Bennett (O). J and K from Byrne & Barker,
1991, with permission; L from Ramofaa et al. 2003. M from Byrne et al. 2003, with permission.)
Thermotolerance of development
There has been considerable interest in the effects of temperature on marine invertebrate devel-
opment, and there is a wealth of data available (ca. 1 sponge, 4 corals, 1 nermertean, 7 molluscs,
20 echinoderms, 2 crustaceans) from developmental, physiological and global change studies across
ontogenetic stages (Table 2). In general, embryos and larvae seem less thermotolerant than gametes/
fertilization (Tables 1 and 2). Studies of the pace of embryogenesis, developmental constraints,
swimming performance, oxygen consumption and planktonic larval duration (PLD) showed that
temperature is the major environmental factor controlling invertebrate development and is a key fac-
tor controlling marine species distributions and recruitment dynamics (Thorson 1950, Kinne 1970,
Pechenik 1987, Hart & Scheibling 1988, Chen & Chen 1992, Roller & Stickle 1993, Hoegh-Guldberg
& Pearse 1995, Young et al. 1998, Gillooly et al. 2002, Staver & Strathmann 2002, McDonald 2004,
Reitzel et al. 2004, O’Connor et al. 2007, Putnam et al. 2008, Compton et al. 2010, Hernández et al.
2010). For many species there is a tight relationship between sea temperature and spawning time,
and this relationship often corresponds to the optimal temperature for larval development (Fujisawa
& Shigei 1990, Johnson & Babcock 1994, Reitzel et al. 2004).
The response of developmental systems to increased temperature is typically seen as a balance
between facilitation at certain levels of warming and developmental failure at upper thermal limits.
This has been documented for sponge, cnidarian, mollusc and echinoderm development (Rupp
1973, Fujisawa 1989, Sewell & Young 1999, Bassim et al. 2002, Negri et al. 2007, Whalan et al.
2008, Byrne et al. 2009, 2011a,b, Byrne 2010, Parker et al. 2010, Sheppard Brennand et al. 2010).
Increased temperature accelerates metabolism up to limits and results in failure when the thermal
stability and function of proteins (e.g., enzymes) are compromised (Somero 2002, 2010, Hofmann
& Todgham 2010, Tomanek 2010).
Moderate warming (≤4°C above ambient/thermal history) is tolerated by the life history stages
of many species (Table 2) with benecial effects of faster growth, larger size and reduced PLD.
Projected near-future ocean warming has been shown to reduce the PLD of sponges, corals and
echinoderms (Putnam et al. 2008, Whalan et al. 2008, Byrne et al. 2011a, Heyward & Negri 2010).
Sea urchin embryos that tolerated a 4°C warming formed normal juveniles with a 25% decrease in
PLD (Byrne et al. 2011a). A shortened planktonic stage may be benecial in increasing retention
of larvae within a region (Byers & Pringle 2006). Reduced PLD also shortens the vulnerable dis-
persive phase when mortality is high (ca. 90%) (Rumrill 1990, Lamare & Barker 1999, Schneider
et al. 2003, Allen 2008). Reduced PLD, however, alters supply side ecology and genetic connectivity
between populations (Shanks et al. 2003, O’Connor et al. 2007).
More extreme ocean warming (≥3–4°C above ambient) is widely deleterious to embryos
(Table 2), as seen in recent studies of coral, oyster and sea urchin development (Byrne et al. 2009,
2011a, Randall & Szmant 2009a, Parker et al. 2010). In the sea urchins Heliocidaris erythrogramma
and Tripneustes gratilla a 6°C warming exceeds developmental thermotolerance (Byrne et al. 2009,
2011a, Rahman et al. 2009, Sheppard Brennand et al. 2010). In response to thermal challenge
the greatest mortality in coral, mollusc and sea urchin embryos occurs prior to or at gastrulation
(Figure 4, Byrne et al. 2009, 2011a,b, Randall & Szmant 2009a). Elevated temperature is also a key
environmental driver of recruitment dynamics and juvenile mortality (Gosselin & Qian 1997, Hunt
& Scheibling 1997, Hernández et al. 2010). Development in extreme thermotolerant species may
not be impaired by projected warming, as seen in the robust response of development in the tropi-
cal sponge Rhopaloeides odorabile and the sea urchin Echinometra mathaei to extreme warming
(8–10°C above ambient) (Rupp 1973, Ettinger-Epstein et al. 2007, Whalan et al. 2008).
The threshold for deleterious warming (degrees above ambient) can vary among developmental
stages within a species (Wright et al. 1983, Byrne et al. 2009, 2010a). For example, early devel-
opment (to gastrulation) in the coral Acropora palmata and the sea urchin Heliocidaris erythro-
gramma, and the trochophore stage in the bivalve Argopecten irradians, is more vulnerable to
warming than later larval stages (Wright et al. 1983, Byrne et al. 2009, 2010a, Randall & Szmant
2009a). Abalone (Haliotis coccoradiata) development appears highly sensitive to warming, with
a small increase (2°C) exerting deleterious effects (Figure 4). Limited thermotolerance seems to
be a general feature of abalone development (Gilroy & Edwards 1998). Coral larvae have limited
thermotolerance, a feature that may be characteristic of coral development (Table 2, Bassim et al.
2002, Randall & Szmant 2009a,b). Increased temperature exerted a major inuence on response
to settlement cues, and larvae changed their preference with 3°C warming (Putnam et al. 2008). In
this case elevated temperature facilitated settlement to an appropriate coralline algal substratum.
Growth in barnacle post-larvae was not affected by increased temperature (4°C above ambient)
(Findlay et al. 2010b).
Developmental thermal thresholds can differ between species even among closely related ones
from similar habitats (Table 2). Experiments with ve sympatric bivalves showed that develop-
ment in some species is highly tolerant to increased temperature (>10°C above ambient), while
others succumbed at a comparatively lower level of increased temperature (1–5°C above ambient)
(Wright et al. 1983). Development in widely distributed intertidal, shallow subtidal and tropical
species and species used for aquaculture (e.g., Crassostrea gigas, Tripneustes gratilla, Echinometra
spp., Heliocidaris erythrogramma) is particularly robust to thermal increase (≥4°C above ambi-
ent, Table 2). A bet-hedging type strategy is evident in corals that produce phenotypically diverse
20°C 22°C 24°C
% Normal cleaving embryo
pH 8.2
pH 8.0
pH 7.8
pH 7.6
Figure 4 Percentage of normal cleavage in the abalone Haliotis coccoradiata in response to ocean change
scenarios for year 2100 (A1F1, IPCC 2007). Both stressors signicantly impaired early development (analy-
sis of variance [ANOVA]: Temperature F2,8 = 10.6, p < 0.001; pH F3,36 = 3.08, p < 0.05) with no interaction
between stressors (n = 8, error bars = standard error of the mean [SEM]). (A) Normal veliger larva from
pH 8.0–8.2/20°C treatments. (B) and (C) Unshelled and abnormal larval phenotypes seen at an increase of
2–4°C above ambient and pH decrease by 0.4 to 0.6 units. Scale = 200 µm.
offspring that differ in their thermotolerance (Putnam et al. 2010). The broad thermotolerance of
embryos and larvae of deep-water echinoids (Stylocidaris lineata, Archaeopneustes histrix) that
live in relatively stable thermal regimes as adults may be associated with migration of larvae into
shallow tropical water during their planktonic phase (Young et al. 1998).
In the warmer part of their range near regions of ocean thermal maxima even robust tropical spe-
cies such as Crossostrea gigas, Tripneustes gratilla or Echinometra spp. may be living at temperatures
near the lethal threshold for development (e.g., Rahman et al. 2009). Reproductive failure of popula-
tions of these and other species living at or near ocean minima and maxima (e.g., equator, poles) may
occur as the ocean warms (Stanwell-Smith & Peck 1998, Tewksbury et al. 2008, Sewell & Hofmann
2011). Adults of several temperate intertidal and coral reef species live on the edge of physiological
thermal tolerance windows (Sagarin et al. 1999, Tomanek & Somero 1999, Sokolova & Pörtner 2001,
Hughes et al. 2003, Pörtner & Knust 2007, Tewksbury et al. 2008, Somero 2010, Tomanek 2010), but
it is not known how this is reected in the thermotolerance of their planktonic stages.
Thermal thresholds of marine propagules are inuenced by adult thermal history (‘environmental
imprinting’), an important consideration when designing stressor experiments. Adult thermal accli-
matization, particularly during egg development, dramatically shifts the thermotolerance of embryos
and larvae (O’Connor & Mulley 1977, Johnson & Babcock 1994, Fujisawa 1995, Bingham et al. 1997,
Byrne et al. 2010a, Zippay & Hofmann 2010a). This developmental plasticity may be due to differences
in maternal loading of protective factors (e.g., heat shock proteins) during oogenesis (Hamdoun & Epel
2007) and may be a source of non-genetic adaptation (phenotypic) to climate change (see p. 25).
With the major controlling inuence that temperature exerts on reproduction in the sea, it is not
surprising that phenological shifts driven by ocean warming are evident in the timing of spawning
and the presence of larvae in the plankton (Edwards & Richardson 2004, Schoeld et al. 2010).
Warming was implicated in a shift in the timing of release of lobster larvae from brooding females,
a change predicted to have a negative effect on larval success (Schmalenbach & Franke 2010).
Phenological shifts driven by ocean warming are creating a trophic mismatch between larvae and
their food, which is a problem for feeding larvae, ecological interactions and planktonic food web
cascades (Philippart et al. 2003, Edwards & Richardson 2004, O’Connor et al. 2009, Schoeld et al.
2010). These shifts are also causing major alterations in benthic-pelagic coupling and changes to
benthic systems (Kirby et al. 2007).
Depending on regional patterns of ocean warming and the seasonal timing of thermal increase
with regard to spawning and planktonic periods, it appears that ocean warming is likely to be
broadly deleterious to core developmental mechanisms (e.g., cleavage, gastrulation, larval mor-
phogenesis) fundamental to development across the Metazoa, with broad implications for marine
ecosystems. It is essential to include regional aspects and adult thermal history when considering
developmental thermotolerance of local populations to identify species at risk, species that may be
resilient in the face of change, and potential for species invasion.
pH/pCO2 tolerance of development
Investigation of the impacts of ocean acidication on development is a burgeoning eld, with data cur-
rently available for about 2 coral, 1 nemertean, 11 mollusc, 14 echinoderm and 7 crustacean species
(Table 2). Of major concern are the fragile skeletons produced by calcifying larvae (Figure 3E–I,O;
Kurihara & Shirayama 2004, Dupont et al. 2008, Kurihara 2008, Byrne 2010, O’Donnell et al.
2010, Parker et al. 2010, Sheppard Brennand et al. 2010, Byrne et al. 2011b). Impaired ability to
produce these skeletons (Figures 4 and 5) and dissolution of skeleton as the ocean decreases in pH
may be the weak link for species persistence. Vulnerability to ocean acidication would lead to
developmental failure of a broad suite of benthic invertebrates.
Because pH, hypercapnia and CaCO3 availability or saturation covary as the ocean absorbs
CO2, it is difcult to separate main factor effects. The decrease in the size of the larval skeleton
observed in many calcifying larvae in response to pH/pCO2 treatments (Table 2 and Figure 5) may
be due to reduced CaCO3 saturation or hypercapnic suppression of metabolic pathways required for
calcication. Regardless of the mechanism involved, production of a smaller larva, reduced growth
rate and production of weaker skeletons will have an impact on swimming and feeding efciency
and increase vulnerability of larvae to predation and physical damage (Allen 2008, Przeslawski
et al. 2008, Soars et al. 2009).
Calcication in marine invertebrates is an ancient evolutionary innovation (ca. 500 million
years ago [mya]), and not surprisingly, major calcifying taxa have different calcication systems
(Porter 2007). The mineral composition of skeletons varies (e.g., calcite or aragonite), and this
difference dictates comparative solubility as mineral saturation states decrease due to ocean
acidication (Doney et al. 2009). Across marine calciers cell and developmental mechanisms of
calcication also differ; this is likely to inuence vulnerability to ocean acidication. For instance,
mollusc veliger larvae develop an aragonite skeleton in ectodermal tissue with its surface in close
contact with surrounding seawater (Figure 3E,F), whereas echinoderm plutei produce a high mag-
nesian calcite skeleton in mesodermal tissue that, due to its internal location, may be more pro-
tected from seawater chemistry (Figure 3G–I). Although details of calcication of the crustacean
exoskeleton still need to be determined (Luquet & Marin 2004), the high organic (chitin, protein)
content of the cuticle of many species may make them more resilient to ocean acidication, as
evidenced by the presence of copepods in highly acidic environments (Derry & Arnott 2007). The
cuticle of marine copepods and amphipods also appear resilient to acidication (Table 2). In crusta-
cean development, vulnerability to decreased CaCO3 saturation would vary greatly between species
and developmental stages with lightly (e.g., copepods, amphipods, larvae, Figure 3O) and heavily
(e.g., lobsters, crabs) calcied exoskeletons (Luquet & Marin 2004, Arnold et al. 2009).
The threshold for negative impacts of ocean acidication on mollusc larval development and
calcication varies among species (Table 2). For bivalves near-future decrease in pH (ca. pH 7.7–7.8;
pCO2 500–800 ppm) resulted in smaller larvae, impaired calcication and delayed metamorphosis
in some species (Crassostrea gigas, C. virginica, Saccostrea glomerata, Argopecten irradiens) but
not in others (Crassostrea ariakensis, Mytilus galloprovincialis) (Table 2). For M. galloprovincia-
lis development to the trochophore stage was normal at pH 7.4 (pCO2 2000 ppm) with deleterious
effects evident in veligers (Kurihara et al. 2008a). Survival of Crassostrea virginica larvae dimin-
ished at pH 7.5 (pCO2 1500 ppm) (Talmage & Gobler 2009). Remarkably, cuttlesh (Sepia ofci-
analis) embryos are able to produce their internal aragonite skeleton under extreme conditions (to
pH 7.1), with increased calcication observed at low pH (Gutowska et al. 2008, 2010a,b).
The impacts of climate change stressors on mollusc embryos developing in benthic egg masses
have been investigated for an intertidal snail, Littorina obtusata, with evidence of sublethal effects
at pH 7.6/pCO2 in chronic long-term (23-day) press experiments (Ellis et al. 2009). These included
24–27°C/pH 7.6
24°C/pH 7.8
27°C/pH 7.824°C/pH 8.2
27°C/pH 8.2
100 µm
Figure 5 Echinopluteus larvae of Tripneustes gratilla reared for 5 days in three pH and two temperature
treatments. Largest larvae were from control pH 8.15/+3°C (27°C) treatments. Acidication (to pH 7.6) and
increased CO2 stunted larval growth, causing a decrease in length of the arms and the supporting skeletal rods.
There was an increase in abnormal development. (See Sheppard Brennand et al. 2010.)
mortality, depressed heartbeat and reduced locomotion (Ellis et al. 2009). Interestingly, these
embryos would experience these conditions in pulse exposures during night-time low tides (Björk
et al. 2004). The calcareous capsular egg masses produced by gastropods (e.g., Nerita spp.) common
on the shore in many regions (Figure 3P) may be vulnerable to low pH. The impacts of environmen-
tal stressors on calcareous egg capsules have not been investigated (Przeslawski 2004).
Abalone (Haliotis coccoradiata) veliger larvae reared from embryos fertilized in experimental
conditions appear particularly sensitive to acidication (Figure 4), with deleterious effects evident
at pH 7.8 and below (Table 2). This sensitivity is also reported for oyster veligers reared from the
outset of development in experimental conditions (Parker et al. 2010).
The pluteus larvae of eight echinoderm species reared in near-future ocean acidication con-
ditions (ca. pH 7.7–7.8) exhibited reduced growth and calcication (Table 2, Figure 5). Increased
acidication and hypercapnia stunt larval growth and produce larvae with shorter arms. Sea urchin
embryos and larvae in ocean acidication treatments also exhibit altered gene expression and changes
to cellular protective biochemistry (O’Donnell et al. 2009, 2010, Todgham & Hofmann 2009).
The impacts of near-future ocean acidication on crustacean development are mixed (Table 2).
In congeneric copepod species (Acartia spp.) neutral and negative effects are reported in larvae
(Kurihara et al. 2004, Kurihara & Isimatsu 2008). In A. erythraea increased mortality is observed
at extreme pH levels well below projected ocean acidication (pH 6.8–7.4, pCO2 10,000 ppm)
(Kurihara et al. 2004). In Calanus nmarchicus hatching success decreased at pH 6.9 (pCO2 8000
ppm) (Mayor et al. 2007). It appears that ocean acidication, even at levels beyond realistic projec-
tions, does not impair development in barnacle, copepod or amphipod larvae (Kurihara et al. 2004,
Kurihara & Ishimatsu 2008, Egilsdottir et al. 2009, McDonald et al. 2009). For lobster development
there was no effect of reduced pH and increased hypercapnia (pH 8.1, pCO2 1200 ppm) in develop-
ment, survival and growth of larvae transferred to experimental conditions as zoea up until the nal
larval stage (Arnold et al. 2009). In nal-stage lobster larvae the mineral content of the carapace was
lower in experimental treatments. This effect was largely attributed to hypercapnia and indicates
poor prospects for the more heavily calcied benthic adult lobster stage (Arnold et al. 2009).
Although data are limited, embryonic (prelarval) stages of species with calcifying larvae and
species that do not have a calcifying stage in their development (Figures 1 and 3) may be more
robust to near-future ocean acidication (ca. < pH 7.8) during their planktonic phase. Three stud-
ies of the effects of near-future acidication on non-calcifying echinoderm larvae showed either
a neutral (Patiriella regularis, Heliocidaris erythrogramma) or a positive (Crossaster papposus)
effect of acidication on larval development and growth (Table 2). This result contrasts with
the miniaturizing effect of decreased pH seen for echinoplutei (Table 2, Figure 5) and suggests
that the decreased pluteal calcication in conditions of ocean acidication is primarily driven
by lowered CaCO3 saturation and less by hypercapnia. Development of planula larvae of coral
species (also lack a skeleton, Figure 3A) is robust to low pH (pH 7.3–7.6) (Kurihara 2008, Suwa
et al. 2010), but in Acropora palmata larval settlement was reduced at pH 7.7–7.8/pCO2 673–998
(Albright et al. 2010). In Acropora digitifera larval metamorphosis was reduced at pH 7.3–7.6
(Table 2). More data are needed on the sensitivity of non-calcifying larvae to ocean acidication
to determine if future outcomes may differ for larvae that have to calcify and those that do not.
Data on the impact of near-future ocean acidication scenarios on postlarvae and early juve-
nile stages are scarce. Reduced larval growth in experimental conditions results in production of
smaller or abnormal juveniles of some coral, barnacle, prawn and sea urchin species (Kurihara
2008, McDonald et al. 2009, Findlay et al. 2010, 2011b, Suwa et al. 2010, Byrne et al. 2011b). In
contrast ocean acidication conditions resulted in an increase in the size of barnacle postlarvae
but at a cost of a weaker skeleton (McDonald et al. 2009). Smaller postlarvae or weaker skeletons
are likely to increase the risk of mortality in the early postlarvae and juveniles. The early benthic
stages can be the major bottleneck in species population dynamics (Gosselin & Qian 1997, Hunt &
Scheibling 1997). Field observations of juvenile mortality and dissolution of juvenile and shells in
low pH estuarine deposits shows that a potential bottleneck in the early benthic stage is a real risk to
successful recruitment and postsettlement survival (Green et al. 2004, Marshall et al. 2008).
Experiments involving transfer of juvenile or adult calciers from contemporary to near-future
ocean acidication conditions in press-type stressor studies reported reduced growth, reduced
calcication, dissolution of skeleton and compromised health in some species (e.g., echinoderms:
Shirayama & Thornton 2005, Miles et al. 2007, Ries et al. 2009; bivalves: Michaelidis et al. 2005,
Gazeau et al. 2007, Bibby et al. 2008; gastropods: Nienhuis et al. 2010; barnacles: Findlay et al.
2010a,b), no change in others (e.g., echinoids: Ries et al. 2009) and reports of increased calcication/
growth in some species (e.g., ophiuroids: Wood et al. 2008; asteroids: Gooding et al. 2009; bivalves:
Range et al. 2011; cuttle sh: Gutowska et al. 2010a; decapod crustaceans: Kurihara et al. 2008b, Ries
et al. 2009). Studies of juvenile bivalves placed in more extreme distant-future ocean acidication
conditions for weeks show broad deliterious effects for oysters (pH 7.5/pCO2 3500) (Beniash et al.
2010) and enhanced growth and survival for clams (pCO2 1698–4344) (Range et al. 2011). The latter
result was attributed to buffering by high local seawater total alkalinity. In 30-week (pH 7.9, pCO2
1000 ppm; pH 7.6, pCO2 1900 ppm) exposure to ocean acidication a decrease in survival of adult
prawns was observed. There was no change in growth of prawns in the pH 7.9 treatments, but at
pH 7.6 a decline in growth was observed after about 6 weeks of incubation (Kurihara et al. 2008b).
It is difcult to assess these highly variable results in the context of future ocean change because
experimental outcomes would be inuenced by age, environmental history and the nutritive status
of the specimens placed in the mesocosms. Some species were fed during experiments (Kurihara
et al. 2008b, Ries et al. 2009, Gutowska et al. 2010a,b), but others were not (Wood et al. 2008).
These studies do, however, provide valuable insights into the dissolution/calcication dynamics of
established juvenile and adult skeletons in ocean change conditions. They indicate that some calci-
ers are more robust than others to ocean acidication. It will be important to conduct long-term
multigenerational experiments on impacts of climate change stressors for ecologically and commer-
cially important species if deleterious effects are not evident early in their life history.
Dissolution of adult bivalve shells in the eld due to inux of low pH water is reported for
Antarctic pteropods, for bivalve shells placed in mesocosms and for species living in and around
naturally acidic (pH 5.4–7.3) vent water (Manno et al. 2007, Hall-Spencer et al. 2008, McClintock
et al. 2009, Tunnicliffe et al. 2009). A signicant reduction in settlement of benthic calciers is
observed at vent sites in the Mediterranean (Cigliano et al. 2010). Studies of deep-sea vent commu-
nities showed mussels living in highly acidic conditions (Tunnicliffe et al. 2009). Although clearly
adapted to living in corrosive low pH conditions, these mussels had weaker shells and would be
more vulnerable to predation than non-vent conspecics with thicker shells (Tunnicliffe et al. 2009).
It has been suggested that the survival of vent mussels in highly acidic conditions requires the pres-
ence of protective periostracum over the shell (Tunnicliffe et al. 2009).
There may be latent effects of exposure to increased acidication and hypercapnia. In experi-
ments in which larval echinoderms, abalone, or adult crabs exposed to pH/ pCO2 treatments were
subsequently challenged with thermal stress, the history of exposure to acidication compromised
thermal tolerance, aerobic ability, cellular defence mechanisms and gene expression with param-
eters measured varying among studies (Metzger et al. 2007, Todgham & Hofmann 2009, O’Donnell
et al. 2010, Zippay & Hofmann 2010b).
Interactive effects of ocean warming and
acidication on fertilization and development
Climate change impacts on invertebrate early life histories have been largely considered in terms of
a single factor, but ocean change involves multiple concurrent factors. In assessing risk to marine life
histories from climate change it is critical to investigate the interactive effects of stressors because
this reects the situation in the real world (Pörtner & Langenbuch 2005, Przeslawski et al. 2005,
2008, Widdicombe & Spicer 2008, Bulling et al. 2010). Environmental stressors can have simple
additive effects (both signicant, but no signicant interaction) or have complex interactive effects
where they have synergistic (increased stress) or antagonistic (decreased stress) effects on biologi-
cal processes (Folt et al. 1999). Despite the well-known controlling inuence of temperature on
development and embryonic thermal thresholds, the interactive effects of ocean warming and CO2-
driven acidication on invertebrate life histories are only documented for a few species. Teasing
out the interactive effects of climate change stressors is a challenge and requires use of factorial
experimental designs.
The interactive effects of concurrent warming and acidication on marine invertebrate life his-
tory stages have been investigated in controlled multifactorial experiments with ve echinoderm,
three mollusc and two crustacean species (Tables 1 and 2, Byrne et al. 2009, 2010a,b, 2011b, Findlay
et al. 2010a,b, Parker et al. 2010, Sheppard Brennand et al. 2010).
Exposure to near-future increased temperature (2 to 4°C) and decreased pH (0.4 to 0.6 pH units)
conditions in all combinations did not impair fertilization in several intertidal and subtidal echinoid,
asteroid and abalone species (Figure 2). There was also no signicant interaction between stres-
sors. In multifactorial experiments that incorporated sperm concentration as a third factor, increased
temperature was expected to facilitate (increase) fertilization at very low sperm concentrations due to
enhanced sperm motility, but hypercapnic narcosis was expected to impair fertilization at low sperm
concentrations (Byrne et al. 2010b). However, neither prediction was borne out (Byrne et al. 2010b).
A study of the interactive effect of temperature (cooling and warming) and pCO2 on fertiliza-
tion in two oysters (Saccostrea glomerata, Crossostrea gigas) found that at the optimal fertili-
zation temperature the percentage of fertilization in both species decreased at low pH (pH 7.8, pCO2
1000 ppm) (Parker et al. 2010).
Resilience of fertilization in many of the shallow-water species listed in Table 1 to climate
change stressors may be due to their adaptation to the uctuating environmental conditions that
they experience in nature. A difference may be seen in multistressor studies with species from more
environmentally stable (subtidal, polar) habitats. However, as mentioned, the confounding inuence
of disparate methodologies used in fertilization studies makes interstudy comparisons difcult.
The interactive effect of ocean warming and acidication on development in marine invertebrates
is poorly understood. On one hand, decreased carbonate saturation and hypercapnia are expected
to impair calcication and suppress metabolism, respectively, whereas elevated temperature would
be expected to enhance developmental processes (up to thermal limits). Some researchers speculate
that warming might stimulate increased calcication through enhancement of physiological pro-
cesses involved and thereby buffer or ameliorate the negative effects of acidication (McNeil et al.
2004). Although this speculation is controversial (see Kleypas et al. 2005, Matear & McNeil 2006),
there is evidence to suggest that low levels of warming diminish the negative effects of acidica-
tion on coral and echinoderm calcication (Kleypas & Yates 2009, Sheppard Brennand et al. 2010,
Byrne 2011b).
Available data from multifactorial experiments of the interactive effects of ocean warming and
acidication/hypercapnia on echinoderm development show that development is highly sensitive to
stress from ocean warming. Surviving larvae and juveniles may be more sensitive to acidication/
hypercapnia due to effects on calcication (Byrne et al. 2009, 2010a, Sheppard Brennand et al.
2010). Temperature is the most important stressor to early embryos (to gastrulation) of the sea
urchin Heliocidaris erythrogramma, with no effect of pH (Byrne et al. 2009, 2011a). There was also
no interactive effect of stressors. Because the echinopluteus larva is reduced in H. erythrogramma
and maternal provisioning is enhanced, the larvae of this species do not need to construct a func-
tional larval skeleton (cf. Figure 3G,N). As a result, development in H. erythrogramma may be
comparatively more robust to acidication stress. For the echinopluteus larva of Tripneustes gratilla
warming accelerated development (up to a threshold), and acidication stunted growth (Figure 5).
A signicant interaction between these stressors indicated that increased temperature diminished
the negative effect of acidication on calcication (Sheppard Brennand et al. 2010). Total larval
calcication was similar in larvae reared at pH 7.8 and 27°C and those reared in control treatments
at pH 8.2 and 24°C (Figure 5). Elevated temperature and acidication both had a negative impact on
skeleton development in juvenile Heliocidaris erythrogramma (Byrne et al. 2011b). The signicant
interaction between the effect of stressors indicted that warming diminished the negative effect of
acidication on spine formation in the early benthic juvenile.
For molluscs, data on the interactive effects of temperature and pH/pCO2 on development are
available for three species (Parker et al. 2010, Byrne et al. 2011b). In two oysters (Crassostrea gigas,
Saccostrea glomerata) and an abalone (Haliotis coccoradiata) the percentage of normal devel-
opment decreased with increasing temperature and acidication in larvae reared in experimental
treatments from the onset of development (Figure 4). Development in the oysters was facilitated
by an increase in temperature (ca. 4°C) but increasing acidication lowered developmental suc-
cess (Parker et al. 2010). In the oyster study, complex synergistic interactions between the effects
of temperature and acidication on development were evident. For abalone, near-future warming
and acidication were both deleterious to development, but there were no interactive effects. A 2°C
warming and 0.4 unit decrease in pH resulted in developmental failure (Figure 4).
In a study of the intertidal barnacle Semibalanus balanoides, warming did not affect growth of
post-larvae while low pH (pH 7.7) negatively impacted growth, with no interaction between stres-
sors (Findlay et al. 2010b).
Multistressor experiments indicated that if the thermal threshold for successful development
is reached in a warm ocean, embryos may not reach the calcifying stage. Thus, depending on the
magnitude of regional warming, the bottleneck for species persistence in local conditions that
are changing due to climate may be embryonic thermotolerance. If embryonic development fails
due to warming, then the question of comprised larval calcication due to acidication may not be
relevant. The impact of climate change on adult organisms means little if development is compro-
mised early in the life cycle.
In addition to data on the impacts of climate change stressors on morphogenesis, empirical data
are also needed on the interactive impacts of climate change stressors on developmental physiol-
ogy and expression of traits important to function and tness. Alteration of individual traits and
sublethal effects (e.g., immune response, respiration, predator detection, sensory ability) not evident
from morphology may also be caused by climate change stressors (Thompson et al. 2002, Sultan
2007, Przeslawski et al. 2008, Munday et al. 2009, Hofmann & Todgham 2010). Physiological
indices of these sublethal responses may be detected using the biomarker (e.g., heat shock and
immune protein expression) or molecular (stress gene expression) approach (Tomanek & Somero
1999, O’Donnell et al. 2009, 2010, Todgham & Hofmann 2009, Nguyen et al. 2011).
There are a few laboratory studies of interactive effects of ocean warming and acidication on the
adult phase and epifaunal communities on settlement plates; these have produced mixed results (e.g.,
corals: Anthony et al. 2008; squid: Rosa & Seibel 2008; seastars: Gooding et al. 2009; brittlestars:
Wood et al. 2010, Christensen et al. 2011; communities: Hale et al. 2011). For instance metabolism was
negatively affected in the squid, whereas growth was positively affected in the seastar. In the brittlestar
Ophiura ophiura metabolic upregulation was observed in low pH treatments (pH 7.3), but a signi-
cant energetic decit was observed as elevated temperature (4–5°C) was introduced (Wood et al.
2010). For this species temperature was the most deleterious stressor. For Ophionereis schayeri
complex interactions between warming and acidication were observed (Christensen et al. 2011).
Field studies of benthic communities living near CO2 vents provided insights into the integra-
tive effects of warming and acidication on benthic invertebrates in the eld (Hall-Spencer et al.
2008, Cigliano et al. 2010, Rodolfo-Metalpa et al. 2010). Growth and calcication of vent fauna in
the Mediterranean were negatively affected by both acidication and warming (Hall-Spencer et al.
2008, Rodolfo-Metalpa et al. 2010), and seasonal comparisons indicated that increased temperature
is of greatest concern (Rodolfo-Metalpa et al. 2010). Insights into potential integrative effects of
warming and acidication are also available from coral cores, where the synergistic inuence of
both stressors decreased the calcication and growth of corals (Cooper et al. 2008). However, these
eld data do not provide details on the extent and nature of stressor interactive effects.
Persistence and potential for acclimatization
and adaptation in a changing ocean
Although placing embryos generated from adults living in present-day conditions into future ocean
conditions is environmentally unrealistic, such experiments do provide insights into stressor tolerance
levels. They also provide useful information for risk assessment with regard to invasive species and
uncertain environmental futures for ecologically (e.g., keystone species) and commercially (e.g., sh-
ery and aquaculture species) important species. Predictive ecological information is needed by man-
agers as they work to mitigate and adapt to likely changes to key marine resources and biodiversity
over the coming decades. With respect to outcomes for marine invertebrates, species will (1) tolerate
change due to their existing phenotypic repertoire; (2) adapt genetically; (3) migrate or (4) undergo
extinction/local extirpation (Peck 2005, Sultan 2007, Przeslawski et al. 2008, Visser 2008, Wethey &
Woodin 2008). The outcome for species populations will be inuenced by all of these responses.
The oceans have been changing gradually for decades, and some regions are changing more than
others (IPCC 2007). Thus it seems likely that some species, populations and faunas have already
experienced some phenotypic and genetic change. Gradual warming in some regions (e.g., south-
eastern Australian waters ca. 2.3°C since 1940; Ridgway 2007) may have promoted increased
thermotolerance in species through gradual acclimatization and selection for tolerant genotypes.
It is well known that progeny from the same parents can exhibit markedly different sensitivities to
stressors, and those that show differential survival represent a subset of tolerant progeny (Galletly
et al. 2007, Byrne et al. 2011a,b). Between-population variation in tolerance to stress is also well
documented (Johnson & Babcock 1994, Bingham et al. 1997, Gaston & Spicer 1998, Kuo & Sanford
2009, Byrne et al. 2011a, Zippay & Hofmann 2010a, Sanford & Kelly 2011). Because the ocean is
changing at a much faster pace than in the geological past, it is not known if adaptive genetic change
can occur at a rate that will avoid local population and species extinctions.
Although the potential for evolution on ecological timescales can be signicant (Levinton et al.
2003, Bridle & Vines 2006, Carroll et al. 2007), clear-cut evidence for evolutionary adaptation to
current climate change stressors appears to be rare (Gienapp et al. 2008). It is not known if the vari-
able expression in stressor tolerance within clutches of embryos from the same parents or within
and between the progeny of different populations is solely due to phenotypic plasticity (diverse phe-
notypes within a single genotype) or if there is some genetic basis to stress tolerance. The potential
contributions of phenotypic plasticity and adaptive heritable variation for species persistence in a
changing ocean can be explored using the tools of quantitative genetics (Hoffmann & Merilä 1999,
Lucas et al. 2006, Evans et al. 2007, Sultan 2007, Foo 2010). This approach may assist in under-
standing potential genetic constraints on adaptive developmental evolution (Sultan 2007).
Stressor tolerance and phenotypic plasticity
Marine invertebrate life histories may be able to tolerate change in the short term if their existing
phenotypic repertoires allow. Phenotypic plasticity provides potential resilience to stressors. An
in-built exibility (polytopy, sensu Hadeld & Strathmann 1996) of life histories to environmental
stress is noted for many marine invertebrates. This polytypy probably increases species persistence
in geological time (Palmer 1994, Hadeld & Strathmann 1996, Davis 2000). In this situation the
phenotype expressed by a given genotype depends on the environmental context in which embryos
and larvae develop, that is, a developmental response system (Sultan 2007). Environmentally con-
tingent phenotypic expression will facilitate persistence of species and populations in the short
term (Sultan 2007). The scope for developmental plasticity is illustrated in the phenotypic response
of sibling sea urchin echinoplutei that alter their feeding structures (larval arms) with respect to
available nutrients (for review see Soars et al. 2009). In benthic-pelagic systems, ocean warming
has promoted wide phenological shifts due to changes in thermal cues for gametogenesis, induction
of spawning and the presence of larvae in the plankton (Hay et al. 2005, Moore et al. 2010). These
changes most likely represent phenotypic adjustments as reproductive systems track environmental
temperature (Giese & Pearse 1974, Olive 1995), rather than genotypic adaptation.
For species with a broad latitudinal distribution, the concept of physiological races of popula-
tions with metabolic temperature compensation to different thermal regimes suggests the presence
of substantial phenotypic plasticity to cope with change (Vernberg 1962, Palmer 1994, Sokolova
& Pörtner 2001, Stillman 2003, Visser 2008, Zippay & Hofmann 2010a, Sanford & Kelly 2011).
Latitudinal differences in the response to heat shock by snail embryos (Nucella ostrina) show that
embryos from cooler climes are less thermotolerant than those from the warmer parts of their range
(Zippay & Hofmann 2010a), but this was not the case for N. canaliculata (Kuo & Sanford 2009).
There was no correlation between thermal tolerance and biogeography for sea urchin development
(Strongylocentrotus purpuratus) in gastrulae or larvae transferred from ambient to experimental
treatments (Hammond & Hofmann 2010). In contrast incubation of sea urchin embryos (Heliocidaris
erythrogramma) from the outset of development indicated that embryos derived from warm-accli-
matized oocytes (from lower-latitude females) are more thermotolerant than those from cooler-
acclimatized oocytes (from higher-latitude females) (Byrne et al. 2011a). The former embryos may
sustain less thermal damage due maternal loading of protective factors into eggs (Hamdoun & Epel
2007) much in the same way that warm-adapted adults are phenotypically more thermotolerant
due to the accumulation of heat shock proteins (Buckley et al. 2001). Broadly distributed species
many also have genotypic variability to facilitate resilience in the face of environmental change
(Bradshaw & Holzapfel 2001, Visser 2008, Kuo & Sanford 2009, Sanford & Kelly 2011).
The adults of some marine invertebrates appear to have considerable acid-base regulation capac-
ity and are able to calcify in what would appear to be extreme conditions (Marshall et al. 2008,
Wood et al. 2008, Tunnicliffe et al. 2009), but there are few data on acid-base regulation for larval
stages (Melzner et al. 2009). Studies of larval cuttlesh showed their considerable ability to calcify
in low pH conditions (Gutowska et al. 2008, 2010a,b). For larval development, data from molecu-
lar studies of development indicate that upregulation of key metabolic and stress genes occurs in
response to warming (corals, Voolstra et al. 2009) and acidication (sea urchins, O’Donnell et al.
2009, 2010, Todgham & Hofmann 2009). It is not known if these changes in gene expression reect
a compensatory adaptive response of the genome or if development is succumbing to stress.
Genetic adaptation
In addition to phenotypic plasticity, variation in success of sibling embryos and larvae to ocean
change stressors may be inuenced by genetic differentiation. As shown for freshwater and terres-
trial invertebrates where environmental stressors select for resistant populations (Bridle & Vines
2006, Derry & Arnott 2007), marine species may have the potential for an adaptive evolutionary
response to climate change. A study of thermal limits in intertidal snails indicted the presence of
thermally tolerant genotypes in different parts of their range (Kuo & Sanford 2009). Rapid genetic-
based adaptation is evident in copepods living in lakes acidied to pH 6.0 for 6–8 years due to SO2
emissions (Derry & Arnott 2007). Contemporary evolution of stress tolerance is also seen in the
genetically based toxicant resistance of a marine oligochaete (Levinton et al. 2003). In the context
of climate change, investigation of potential for evolutionary adaptation of marine life histories at
range margins and in warming hot spots may be particularly informative (e.g., Bridle & Vines 2006,
Somero 2010, Tomanek 2010).
Adaptive changes reect an integrated response to multistressors (Harley et al. 2006) and will
be inuenced by generational turnover time. Short-lived species with fast generation times (e.g.,
temperate copepods, amphipods) are likely to have a greater capacity for evolutionary adaptation
to climate change than slow-developing species (e.g., polar species, Smale & Barnes 2008, Fabry
et al. 2009). For long-lived species with slow development and long generation times population
bottlenecks may exacerbate the problem by reducing genetic variation and limit the scope for an
evolutionary response.
Many marine species originated under very different conditions compared with those they
experience in their present-day situation, suggesting that some species are ‘exapted’ rather than
‘adapted’ per se to modern conditions (Jackson & Johnson 2000). Persistence of species through
past extinction events and climate change indicates adaptive capacity across the ontogenetic stages
of some species through past climate change (Jackson & Johnson 2000, Uthicke et al. 2009).
Larval migration, range extensions, faunal replacements and extinction
Long-term studies of planktonic larval stages and adult distribution showed that warm-water species
extend ranges during warmer periods, whereas colder-water species decline (Southward et al. 1995,
Thompson et al. 2002, Wethey & Woodin 2008), although survival patterns of resident species and
those that arrive in warm ocean conditions can be complex and contrary to expectations (Schiel
et al. 2004). Because new corridors for larval dispersal are being created by ocean warming and
changes in circulation, a number of species are exhibiting poleward range shifts as the opportunity
and favourable conditions arise (Thatje et al. 2005, Jones et al. 2009, Ling et al. 2009). Range shifts
in response to climate change can also be vertical, that is, shallower or deeper, or to different levels
in the intertidal zone (Hellberg et al. 2001, Helmuth et al. 2006, Harley & Paine 2009). Patterns in
distribution shifts are complex and are likely to be inuenced by many environmental factors, with
gradual and punctuated changes observed (Harley & Paine 2009).
Range shifts provide a mechanism for some species to escape degenerating conditions due to
warming in their normal range. Thus some species may have the potential to keep up with a warm-
ing world through poleward migration of thermotolerant propagules and a contraction in warmer
parts of their range (Visser 2008, Byrne et al. 2011a). Warm-adapted conspecics from warming
hot spots are also a potential source of thermotolerant propagules to maintain populations (Somero
2010, Tomanek 2010). Prospects appear dire for cold-water, high-latitude species that have little
scope to migrate, and extinctions are predicted (Peck 2005, Barnes & Peck 2008, Fabry et al. 2009,
Mueter & Litzow 2009, Sewell & Hofmann 2010, Somero 2010, Tomanek 2010). Low-latitude tropi-
cal species and species along the intertidal margin are similarly vulnerable (Przeslawski et al. 2008,
Tewksbury et al. 2008, Harley & Paine 2009).
Where poleward invasions have occurred, major ecosystem changes have ensued, particularly
where keystone species are involved. Examples are the invasive predatory crab (Lithodes confun-
dens) to Antarctica and the ‘barrens’-forming sea urchin (Centrostephanus rodgersii) to Tasmania
(Thatje et al. 2005, Ling et al. 2009). These invasions are resulting in loss of biodiversity and local
extinctions. The interactive effects of multiple stressors and the complexities of biological and eco-
logical responses (Schiel et al. 2004, Przeslawski et al. 2008) however make it a challenge to predict
future outcomes. For instance, larvae of the sea urchin C. rodgersii and other calcifying larvae in
south-eastern Australia may migrate poleward, a process facilitated by increased warming and
southerly ow of the East Australian Current, but may face a developmental bottleneck as acidied
waters with low mineral saturation expand northward in the Southern Ocean (Richardson et al.
2009, Byrne et al. 2011a).
Thermotolerant frontier tropical, warm temperate and subpolar larvae appear to have the great-
est potential to migrate and increase their range in a changing ocean, with species persisting and
successfully reproducing in their new habitats (Thatje et al. 2005, Przeslawski et al. 2008, Ling
et al. 2009, Figueira & Booth 2010, Parker et al. 2010). Some species introduced for aquaculture
(e.g., Crossostrea gigas) are likely to be particularly dominant in the future and will outcompete
endemic species with more sensitive developmental stages (Parker et al. 2010). Species such as the
invasive crab Carcinus maenus (see deRivera et al. 2007, Compton et al. 2010) with large latitudinal
distributions across broad thermal ranges may have an in-built adaptive capacity across ontogenetic
stages (fertilization to adult) to survive and migrate in a changing ocean. Related narrow-range
species by contrast are likely to be more sensitive and may go extinct as their more tolerant rela-
tives replace them. This scenario conveys the possibility of ecological redundancy in losses and
gains of species that may perform similar ecological functions. Although the copepods in acidied
lakes were able to rapidly adapt to a changing environment, most of their associated species were
extirpated (Derry & Arnott 2007). Signicant loss of marine biodiversity due to climate change
stressors seems inevitable.
Evolution of life history modes in a changing ocean
Over evolutionary time many invertebrate clades have deleted a pelagic stage from their life history
or have switched from possessing a planktotrophic feeding larva (e.g., Figure 3G–L) to a lecitho-
trophic non-feeding larva (e.g., Figure 3M,N) (Valentine & Jablonski 1986, Pechenik 1999, Raff &
Byrne 2006, Uthicke et al. 2009). Marine invertebrates may have evolved a buffered non-feeding
larval life history, free of the vagaries of planktonic food supply in response to stressful condi-
tions in the plankton, including past climate change (Valentine & Jablonski 1986, Pechenik 1999,
Uthicke et al. 2009). Signicant maternal provisioning in benthic or pelagic progeny provides a
buffer against stress by eliminating the need to feed (Figure 3M,N). By contrast, feeding larvae are
vulnerable to disruption of planktonic food webs caused by ocean warming, and those that need to
calcify will face difculties in producing their fragile skeleton (Figure 3G–I) as carbonate satura-
tion decreases (Philippart et al. 2003, Edwards & Richardson 2004, Kurihara 2008, Clark et al.
2009, Byrne 2010, Parker et al. 2010, Sheppard Brennand et al. 2010).
For the crab Lithodes confundens currently undergoing poleward migration, larval lecithotro-
phy and cold tolerance may have enabled them to conquer polar ecosystems (Thatje et al. 2005). A
meta-analysis of larval type and extinction risk over evolutionary history indicated that echinoderm
species with non-feeding, non-calcifying larvae and short development times were more resilient to
extinction driven by climate change than species with feeding larvae (Uthicke et al. 2009). In major
echinoderm groups there has been differential extinction of species with planktotrophic develop-
ment through past climate change (Valentine & Jablonski 1986, Uthicke et al. 2009). As seen in the
asterinid seastars and temnopleurid echinoids, once echinoderm clades evolve lecithotrophic devel-
opment this process is irreversible, and subsequent species radiation generates other lecithotrophic
developers (Jeffery et al. 2003, Byrne 2006).
Different outcomes for regional faunas and habitats
As detailed in the previous discussion, there are signicant differences between species and life
history stages in tolerance to ocean change stressors (Tables 1 and 2). These differences are even
seen among closely related sympatric species. The weight of evidence (Tables 1 and 2) indicates
that life history stages of widely distributed midlatitude intertidal, estuarine and shallow subtidal
species may tolerate near-future levels of ocean warming and acidication. Many of these species
have a wide physiological tolerance, and some have behavioural and morphological strategies to
cope with temperature, pH and other climate change stressors (e.g., salinity, ultraviolet [UV] radia-
tion) (Thompson et al. 2002, Przeslawski 2004, Przeslawski et al. 2005, 2008, Przeslawski & Davis
2007). A review of the responses of rocky shore communities to environmental stressors attests to
their remarkable resilience to perturbation (Thompson et al. 2002). Coastal and shallow water spe-
cies as thermal generalists (sensu Pörtner & Knust 2007) may have preadaptive traits to buffer them
against ocean change.
In the context of ocean warming and acidication, intertidal and shallow-water temperate species
already experience marked uctuations in environmental pH (ca. pH 6.9–10.1) and hypercapnia due to
the diel interplay between respiration and photosynthesis and experience marked temperature uctua-
tion (ca. 12°C) due to tidal exchange (Truchot & Duhamel-Jouve 1980, Morris & Taylor 1983, Ringwood
& Keppler 2002, Björk et al. 2004, Wootten et al. 2008). These changes in environmental stressors far
exceed the changes anticipated for global ocean surface waters in the next 100–200 years.
The pH of body uids of intertidal invertebrates across eight phyla (23 species) measured at
low tide ranged from pH 6.8 to pH 7.8 with the coelomic uid of echinoderms being acidic (pH
6.8–7.0) (Mangum & Shick 1972, Punzo 1977). However, physiological acidosis and warming in
the intertidal are experienced as limited duration pulse stressors at low tide. If warming and acidi-
cation become permanent press-type stressors then even robust intertidal species may be less
able to withstand these conditions. Newly settled juveniles with developing skeletons (Figure 3Q,R)
are particularly vulnerable (Arnold et al. 2009, Cigliano et al. 2010, Byrne et al. 2011b). Although
the physiological tolerance of shallow-water and coastal species may be a preadaptive feature facili-
tating persistence of benthic stages (juveniles, adults) faced with ocean change, this is likely to incur
increased energetic cost of metabolism (Porter 2007, Pörtner 2008, Widdicomb & Spicer 2008,
Hofmann & Todgham 2010).
For faunas of other habitats and regions the potential outcomes of ocean change appear more
serious. The developmental stages of thermal specialists from stable low- and high-latitude envi-
ronments and stenothermal habitats (e.g., poles, equator, deep water) have low scope to tolerate
climate change stressors (Stanwell-Smith & Peck 1998, Pörtner & Knust 2007, Przeslawski et al.
2008, Smale & Barnes 2008, Tewksbury et al. 2008). Shallowing of CaCO3 horizons is a concern
for deep-water species, and fast warming is a concern for stenothermal species (Turley et al. 2007,
Barnes & Peck 2008, Smale & Barnes 2008, Fabry et al. 2009, Sewell & Hofmann 2010). The fate
of ecosystems based on structure and habitats generated by biogenic CaCO3 such as shallow- and
deep-water coral reefs seems perilous (Hoegh-Guldberg et al. 2007, Turley et al. 2007, Veron 2009).
In this case, the potential for developmental adaptation may be irrelevant if their habitat and key
associated species (e.g., prey) are compromised. Major habitat change caused by the demise of an
ecosystem engineer is seen in the periodic disappearance of corals and associated biota from the
fossil record due to ocean warming and acidication and the likely decalcication of corals (Fine &
Tchernov 2007, Veron 2009, Kiessling & Simpson 2011).
Conclusion: developmental success in a multistressor world
This review focuses on two stressors: warming and acidication. Although these are the key pres-
ent-day climate change stressors that affect the life histories of marine invertebrates (Pörtner et al.
2004, Pörtner & Langenbuch 2005), this generalization is an oversimplication. Marine propagules
are exposed to multiple stressors from climate change (e.g., salinity, changed disease dynamics, UV
radiation) and other anthropogenic inuences (e.g., overshing, pollution), and these stressors are
unlikely to act independently (Przeslawski et al. 2005, 2008, Harley et al. 2006, Crain et al. 2008,
Byrne 2010). For instance elevated temperature and decreased pH are both well known to exacer-
bate the toxicity of pollutants (e.g., metals) to life history stages and the performance of key biomol-
ecules (e.g., enzymes) (MacInnes & Calabrese 1979, Knutzen 1981, Cotter et al. 1982, McLusky
et al. 1986, Byrne et al. 1988, Millero et al. 2009). Climate change stressors are exacerbating the
demise of already-stressed species and ecosystems. Ecosystem resilience will strongly inuence
future outcomes for species and communities (Thompson et al. 2002, Hughes et al. 2003, Harley
et al. 2006, Przeslawski et al. 2008, Brierley & Kingsford 2009).
Understanding the vulnerabilities of marine life history stages is crucial as we endeavour to
predict how marine populations and ecosystems will fare in the face of climate change. If develop-
ment is compromised at an early stage in the life history (Figure 1), downstream consequences are
likely to result in local extinction of species. There is an urgent need for multifactorial studies to
assess fates for marine biodiversity under uncertain environmental futures (Bulling et al. 2010).
Determination of the potential for phenotypic and genotypic adaptation in a changing ocean is
crucial to identify potential ‘winners and losers’ in the climate change stakes. This is especially
important for abundant and ecologically important species in marine ecosystems (Harley et al.
2006, Brierley & Kingsford 2009).
Earth has entered a new phase in its history, experiencing a pace of climate change far greater
than the planet has experienced over evolutionary timescales. Predicting the outcome of the interac-
tive effect of these stressors for marine biota remains a signicant challenge.
This work was supported by a grant from the Australian Research Council. Contribution #49 Sydney
Institute of Marine Science. Assistance was provided by P. Cisternas, S. Dworjanyn, H. Sheppard
Brennand and N. Soars. Thanks are due to R. Babcock, B. Degnan, I. Bennett, L. Page and E. Wong
for the use of their images. Thanks to S. Dworjanyn, R. Gibson and M. Lamare for comments on
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... Cette modification de la température des eaux a de nombreux effets sur les espèces marines. Une modification de la température des eaux peut modifier la distribution des espèces en fonction de leur préférence bioclimatique (Raitsos et al., 2010;Hastings et al., 2020), mais également modifier leur rythme physiologique (Brierley and Kingsford, 2009;Byrne, 2011). Cette modification des rythmes physiologiques des espèces peut être soit lié à une modification du métabolisme des espèces (effet de la température sur la cinétique métabolique des espèces) ou bien à un dérèglement des rythmes saisonniers des espèces, de par une modification des températures saisonnières. ...
... Losing this ability makes a system less resilient to stressors, as described by . It is well known that invertebrates are going to be highly impacted by CC (Kendall et al., 2004;Byrne, 2011). However, few studies have investigated the overall effect of community changes on ecosystem functioning. ...
Avec l’accroissement de la population humaine sur Terre, le nombre et l’intensité des activités humaines sur les littoraux ne cessent d’augmenter. Ces activités peuvent avoir des effets importants sur l’environnement et sur les écosystèmes. De plus, la grande diversité de ces activités sur les côtes fait que les écosystèmes côtiers sont presque toujours soumis à de multiples facteurs de changements d’origine humaine. Ces facteurs peuvent interagir entre eux, provoquant des effets dit cumulés, qui peuvent avoir des conséquences importantes, et difficilement prévisibles, sur les écosystèmes. C’est dans le cadre du développement des énergies marines renouvelables en France, que cette thèse met en place des méthodes innovantes pour quantifier les effets séparés et combinés de multiples facteurs de changements, comprenant : le futur parc éolien de Courseulles-sur-Mer, le changement climatique, et l’effet du Brexit sur les régimes de pêche. Les effets combinés de ces facteurs sur le fonctionnement et la résilience de l’écosystème de la baie de Seine ont été quantifiés avec l’aide d’approches écosystémiques holistiques.Nos résultats indiquent que les mécanismes d’interactions des facteurs sont complexes et multiples,néanmoins les potentiels effets structurants des facteurs sur le fonctionnement des écosystèmes jouent un rôle déterminant sur la genèse des effets cumulés. Les effets cumulés apparaissent hétérogènes entre les propriétés fonctionnelles des écosystèmes et spécifiques aux écosystèmes étudiés. Il est donc important de réaliser des études fonctionnelles du cumul de multiples facteurs à des échelles locales, pour déterminer les effets de l’homme sur les écosystèmes, et vice versa, en prenant en compte les multiples services rendus par les écosystèmes.
... Some older reviews may pre-date bibliometric information retrieval and not feature in this list. Interestingly and coincidentally, members of the current (and recently expanded) editorial board feature in this list (Hawkins & Hartnoll 1983, Byrne 2011. The current board also has several members who have contributed to OMBAR in the past and/or in this volume. ...
... Looking back over the top-cited papers over the last 10-year period (2009-2019, Table 2), the current board (Vol. 60) features again with Firth et al. (2016), Todd via Neo et al. (2017), Byrne again in addition to Byrne (2011) via Purcell et al. (2016. It is clear from Table 2 that a diversity of topics are covered in OMBAR reviews, including historical ecology (Lotze 2010). ...
... The rate of larval development and planktonic larval duration have positive and negative relationships with temperature, respectively, up to a limit when deleterious effects occur due to stress and mortality (Byrne, 2011). In sea urchins, early embryos are often tolerant of increased temperature (Byrne et al., 2009O'Donnell et al., 2009) potentially due to the presence of protective maternal factors that diminish throughout development with mortality increasing at the later stages (Hamdoun & Epel, 2007). ...
... , the trade-offs were evident with the alterations in size and development rates of the offspring. As typical of sea urchins, and marine invertebrates in general(Byrne, 2011;, temperature increased the progression of the H. erythrogramma larvae through developmental stages. Only when strong conditions were sustained did the cross-generational legacy of heat stressed parents result in eventual high mortality. ...
With rising ocean temperatures, extreme weather events such as marine heatwaves (MHWs) are increasing in frequency and duration, pushing marine life beyond their physiological limits. The potential to respond to extreme conditions through physiological acclimatization, and pass on resistance to the next generation, fundamentally depends on the capacity of an organism to cope within their thermal tolerance limits. To elucidate whether heat conditioning of parents could benefit offspring development, we exposed adult sea urchins (Heliocidaris erythrogramma) to ambient summer (23°C), moderate (25°C) or strong (26°C) MHW conditions for 10 days. Offspring were then reared at constant temperature along a thermal gradient (22-28°C) and development was tracked to the 14-day juvenile stage. Progeny from the MHW-conditioned adults developed through to metamorphosis faster than those of ambient conditioned parents, with most individuals from the moderate and strong heatwaves developing to the larval stage across all temperatures. In contrast, the majority of offspring from the control summer temperature died before metamorphosis at temperatures above 25°C (moderate MHW). Juveniles produced from the strong MHW-conditioned adults were also larger across all temperatures, with the largest juveniles in the 26°C treatment. In contrast, the smallest juveniles were from control (current-day summer) parents (and reared at 22 and 25°C). Surprisingly, initial survival was higher in the progeny of MHW exposed parents, even at temperatures hotter than predicted MHWs (28°C). Importantly, however, there was substantial mortality of juveniles from the strong MHW parents by day 14. Therefore, while carryover effects of parental conditioning to MHWs resulted in faster growing, larger progeny, this benefit will only persist beyond the more sensitive juvenile stage and enhance survival if conditions return promptly to normal seasonal temperatures within current thermal tolerance limits.
... Population distribution is influenced by animal fitness through different life stages (Byrne and Przeslawski 2013), especially for species with biphasic life cycles. Both acclimation potential and environmental tolerance limits can vary with ontogeny and age in marine ectotherms (Byrne 2011;Freda et al. 2019). For example, post-settlement juvenile mussels, referred to as "recruits", often have a higher capacity for rapid phenotypically plastic responses to temperature (Lou et al. 1982;Gleason et al. 2018) as compared to adults. ...
Full-text available
For marine animals with biphasic life stages, different environmental conditions are experienced during ontogeny so that physiological constraints on early stages could explain adult distributions and life history traits. The invasive and cool-temperate adapted Mytilus galloprovincialis intertidal mussel approaches the eastern limit of its biogeographic distribution on the south coast of South Africa, where it shares a habitat with the warm-temperate adapted and indigenous Perna perna mussel. As adults, the two species exhibit different metabolic regulation capacities in response to temperature. We compared the acute metabolic response to temperature between species during the post-settlement recruit stage. Aerobic respiration rates of recently settled recruits were measured monthly for 5 months for temperatures 5 °C above or below the ambient field seawater temperature at the time of collection. Unlike adults, the capacity for aerobic metabolic regulation in response to temperature differed little between species under the conditions tested, indicating a similar degree of phenotypic or developmental plasticity in response to the thermal environment. In addition, monthly variations in metabolic patterns indicate unexpectedly high plasticity in response to recent seasonal thermal history for both species.
... Early life-history stages are known to be more sensitive to climate stressors (Walther et al., 2010;Byrne, 2011;Quinn, 2017). Since larvae thermal tolerance is strongly dependent on embryo temperature acclimatation (Diaz, 1987;Miller et al., 2013;Mueller et al., 2019), during MHWs larvae may be exposed to higher temperatures than those where they acclimated during the incubation phase, which may decrease their resilience and survivorship to critical levels. ...
Climate change is imposing constant and more severe environmental challenges to coastal and marine species. Regional climate and species acclimation capacity determine the communities' ecological response to stressors. Marine heatwave events are of serious threat to species fitness and survivorship, even more to the sensitive early-history stages of ectotherms. By combining modeled regional historical data and climate change predictions with manipulative experiments, we evaluated the potential impact of marine heatwaves in a widespread and abundant planktonic larvae of the fiddler crab Leptuca thayeri. Larvae survival was affected by temperature increase with lowest survival probability under higher temperature treatments regardless of pH conditions. Larval physiology was affected by both temperature increase and pH conditions. With heatwaves becoming more frequent, hotter, and lasting longer in the region, we could expect potential reductions in the larval recruitment and stocks with cascade ecological negative effects on estuarine habitats.
... proved to supply hundreds of species to recruit to the mesocosms over the course of this experiment 50 . Second, as warming has been shown to increase growth and recruitment in some studies 60,61 , the average increase in temperature of 0.64 °C within the mesocosms (Supplementary Figure S1) could have augmented recruitment to the mesocosms. However, Timmers et al. (2021) found that sponge diversity was unaffected by a + 2 °C warming, making it unlikely that warmer temperatures in the mesocosms were responsible for the differences observed here. ...
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Successional theory proposes that fast growing and well dispersed opportunistic species are the first to occupy available space. However, these pioneering species have relatively short life cycles and are eventually outcompeted by species that tend to be longer-lived and have lower dispersal capabilities. Using Autonomous Reef Monitoring Structures (ARMS) as standardized habitats, we examine the assembly and stages of ecological succession among sponge species with distinctive life history traits and physiologies found on cryptic coral reef habitats of Kāneʻohe Bay, Hawaiʻi. Sponge recruitment was monitored bimonthly over 2 years on ARMS deployed within a natural coral reef habitat resembling the surrounding climax community and on ARMS placed in unestablished mesocosms receiving unfiltered seawater directly from the natural reef deployment site. Fast growing haplosclerid and calcareous sponges initially recruited to and dominated the mesocos